Phytobiomes: Current Insights and Future Vistas [1st ed.] 9789811531507, 9789811531514

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Manoj Kumar Solanki Prem Lal Kashyap Baby Kumari   Editors

Phytobiomes: Current Insights and Future Vistas

Phytobiomes: Current Insights and Future Vistas

Manoj Kumar Solanki  •  Prem Lal Kashyap  •  Baby Kumari Editors

Phytobiomes: Current Insights and Future Vistas

Editors Manoj Kumar Solanki Department of Food Quality & Safety Institute for Post-harvest and Food Sciences, The Volcani Center, Agricultural Research Organization

Rishon LeZion, Israel

Prem Lal Kashyap Division of Crop Protection Indian Institute of Wheat and Barley Research Karnal, Haryana, India

Baby Kumari Department of Biotechnology Vinoba Bhave University Hazaribag, Jharkhand, India

ISBN 978-981-15-3150-7    ISBN 978-981-15-3151-4 (eBook) https://doi.org/10.1007/978-981-15-3151-4 © Springer Nature Singapore Pte Ltd. 2020 This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors, and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, expressed or implied, with respect to the material contained herein or for any errors or omissions that may have been made. The publisher remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. This Springer imprint is published by the registered company Springer Nature Singapore Pte Ltd. The registered company address is: 152 Beach Road, #21-01/04 Gateway East, Singapore 189721, Singapore

Preface

This book addresses the updates about the plant-associated microbiomes and their contemporary uses. To satisfy the food demands of the global population, advanced technology-based research is needed that can extract the information from the plant metabolism and microbial gene pools up to the complexity. Modern biotechnological tools can unlock the limitations of agricultural practices. However, the application of these tools is not well-equipped. Eco-friendly agriculture using microbial inoculants had positive influences on soil/plant health. Exploring the plant-­ associated microbial niches, especially endophytes, epiphytes, and soil microbes and how they are benefitting each other, can open new insights to develop sustainable agriculture practices by using consortia of microbes as plant helpers that recover the imbalanced agriculture systems and manage pathogenic diseases. This book inculcates the gap between soil and plant helper microbiomes and their importance in the intensification of sustainable agriculture. New insights of phytobiome are explored in various chapters on a variety of interrelated aspects of the fascinating areas like plant microbial interaction, integrated pest management, soil fertility intensification, sustainable crop production, and disease management. This book is also entitled to yield a plethora of information about how beneficial plant microbiomes are currently being utilized for smart farming practices. To resolve the global food problem without harming the soil and environment health, this book covers valuable information regarding the significance of microbes in the amelioration of plant and soil health. Application of advanced molecular tools in plant disease diagnosis and pathogen isolation has also been discussed in order to advance the crops and human health. Some chapters have also been written to present the latest information related to phytobiomes and their range as far as their utility is concerned. Information on plant health promoter, endophytes as microbial elicitors, fly ash and plant health, zinc solubilizers, and their role in ecosystem engineering towards sustainable agriculture have also been presented. This book is intended for everyone who is directly or indirectly involved in agriculture, bioinformatics, and all disciplines related to microbial biotechnology. These include academicians, scientists, and researchers at universities, institutes, industries, and government organizations who want to understand microbial linkages in a shorter time. This book also contains essential information that will help the nonspecialist readers to understand progressive research. We are confident that the current edition will be a milestone as chapters having updated information are v

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anticipated to be published in Phytobiomes: Current Insights and Future Vistas. The views conveyed by the expert/authors in their respective chapters are based on their vast experience in the plant-microbe interaction and associated research areas. We thank all the contributors to this book, and we are obliged for their valuable contributions. Rishon LeZion, Israel Karnal, Haryana, India Hazaribag, Jharkhand, India

Manoj Kumar Solanki Prem Lal Kashyap Baby Kumari

Contents

1 Phytobiomes: Role in Nutrient Stewardship and Soil Health����������������   1 Madhumonti Saha, Abhijit Sarkar, Trisha Roy, Siddhartha Shankar Biswas, and Asit Mandal 2 Role of a Quorum Sensing Signal Acyl-­Homoserine Lactone in a Phytobiome ��������������������������������������������������������������������������  29 Pushparani D. Philem, Avinash Vellore Sunder, and Sila Moirangthem 3 Plant Microbiomes: Understanding the Aboveground Benefits������������  51 Mohini Prabha Singh, Pratiksha Singh, Rajesh Kumar Singh, Manoj Kumar Solanki, and Sumandeep Kaur Bazzer 4 Plant Mycobiome: Current Research and Applications������������������������  81 Ajit Kumar Dubedi Anal, Shalini Rai, Manvendra Singh, and Manoj Kumar Solanki 5 Role of Soil Fauna: En Route to Ecosystem Services and Its Effect on Soil Health �������������������������������������������������������������������� 105 Apurva Mishra and Dharmesh Singh 6 An Insight into Current Trends of Pathogen Identification in Plants������������������������������������������������������������������������������ 127 Vinay Kumar, Vinukonda Rakesh Sharma, Himani Patel, and Nisha Dinkar 7 Linkages of Microbial Plant Growth Promoters Toward Profitable Farming������������������������������������������������������������������������������������ 163 Priyanka Verma, Anjali Chandrol Solanki, Manoj Kumar Solanki, and Baby Kumari 8 Wheat Microbiome: Present Status and Future Perspective ���������������� 191 Sunita Mahapatra, Pravallikasree Rayanoothala, Manoj Kumar Solanki, and Srikanta Das

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9 Entomopathogenic Fungi: A Potential Source for Biological Control of Insect Pests ������������������������������������������������������������������������������ 225 Anjney Sharma, Ankit Srivastava, Awadhesh K. Shukla, Kirti Srivastava, Alok Kumar Srivastava, and Anil Kumar Saxena 10 Role of Microbiotic Factors Against the Soil-Borne Phytopathogens������������������������������������������������������������������������������������������ 251 Nasreen Musheer, Shabbir Ashraf, Anam Choudhary, Manish Kumar, and Sabiha Saeed 11 Zinc-Solubilizing Microbes for Sustainable Crop Production: Current Understanding, Opportunities, and Challenges���������������������� 281 Prity Kushwaha, Prem Lal Kashyap, K. Pandiyan, and Ajay Kumar Bhardwaj 12 Endophytic Phytobiomes as Defense Elicitors: Current Insights and Future Prospects��������������������������������������������������� 299 Satyendra Pratap Singh, Arpita Bhattacharya, Rupali Gupta, Aradhana Mishra, F. A. Zaidi, and Sharad Srivastava 13 Role of Biotechnology in the Exploration of Soil and Plant Microbiomes������������������������������������������������������������������������������ 335 Akhilendra Pratap Bharati, Ashutosh Kumar, Sunil Kumar, Deepak K. Maurya, Sunita Kumari, Dinesh K. Agarwal, and S. P. Jeevan Kumar 14 Plant-Parasitic Nematode Management by Phytobiomes and Application of Fly Ash������������������������������������������������������������������������ 357 Gufran Ahmad, Mohammad Haris, Adnan Shakeel, Abrar Ahmad Khan, and Asgar Ali 15 Phytobiome Engineering and Its Impact on Next-Generation Agriculture�������������������������������������������������������������������������������������������������� 381 Baby Kumari, Mahendrakumar Mani, Anjali Chandrol Solanki, Manoj Kumar Solanki, Amandeep Hora, and M. A. Mallick

About the Editors

Dr. Manoj  Kumar  Solanki Ph.D. (Microbiology) is working as a visiting scientist at the Volcani Center, Agricultural Research Organization, Israel. He was awarded a visiting scientist fellowship from the Guangxi Academy of Agriculture Sciences, China, and a senior research fellowship from the Indian Council of Agriculture Research (ICAR), India. He also worked as a Research Associate at the International Crops Research Institute for the Semi-Arid Tropics (ICRISAT), India in a Department of Biotechnology funded project. He has engaged in various research activities on plant-microbe interactions, soil microbiology, plant disease management, and enzymology, and has published several book chapters and research papers in prominent international journals.  

Dr. Prem  Lal  Kashyap Ph.D. (Plant Pathology) is working at the ICAR-Indian Institute of Wheat and Barley Research (IIWBR), India. His major research areas include wheat pathology, biocontrol, diagnostics, microbial nanotechnology and host–parasite interactions. He has published over 60 research papers in high impact factor journals along with several book chapters, technical bulletins and books. In recognition of his significant achievements in the field of crop protection, he has received several prestigious awards including the NAAS Young Scientist Award, Dr. Basant Ram Young Scientist Award, Prof.  Abrar Mustafa Memorial Award, M.K.  Patel Memorial Young Scientist Award, and a NAAS Associateship at the national level.  

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About the Editors

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Dr. Baby  Kumari MSc, Ph.D. (Biotechnology) has worked as a researcher (part of her Ph.D. work) at the Bhabha Atomic Research Centre, India. She has engaged in various research activities on plant-microbe interactions, soil microbiology, plant disease management, and nanotechnology, and has published many research papers in prominent international journals. Her research interests include plant-microbiome interactions, especially in medicinal plants, as well as nanoparticle biosynthesis and its application in plant disease management, biosensors, and bioremediation.  

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Phytobiomes: Role in Nutrient Stewardship and Soil Health Madhumonti Saha, Abhijit Sarkar, Trisha Roy, Siddhartha Shankar Biswas, and Asit Mandal

Abstract

The enormous potential of the phytobiome for better plant growth and productivity is an essential tool for sustainable agronomic practices for eco-friendly cultivation processes. However, microbes in relation to plants, environment, omics, and their interactions are still to be clearly explored. Current predictive formulae like niche origin, ecological traits, evolution, genetics or heterosis, and resource trades are not mutually exclusive. This chapter mainly emphasizes on phytobiome related to soil fertility, nutrient cycling, plant growth, and soil health. Plant-­ associated phytobiome such as rhizospheric and phyllospheric played a significant role in the enhancement of plant growth and yield. These organisms form multifarious networks that are established and regulated through nutrient cycling, competition, antagonism, and chemical communication mediated by a diverse array of signaling molecules. The integration of knowledge of signaling mechanisms with that of phytobiome members and their networks will lead to a new understanding of the fate and significance of these signals at the ecosystem level. Such an understanding could lead to new biological, chemical, and breeding strategies to improve crop health and productivity. Soil organic matter (SOM) is a heterogeneous mixture of materials that range in the stage of decomposition from fresh plant residues to highly decomposed material known as humus. SOM is made of organic compounds that are highly enriched in carbon. Though half of the global population depends on fertilizer N, atmospheric N fixation by rhizospheric microbes is essential for plant productivity in low N soils. Many plants form symbiotic associations between their roots and specialized fungi in the soil M. Saha · A. Sarkar (*) · A. Mandal ICAR-Indian Institute of Soil Science, Bhopal, Madhya Pradesh, India T. Roy ICAR-Indian Institute of Soil and Water Conservation, Dehradun, Uttarakhand, India S. S. Biswas ICAR-National Research Centre for Orchids, Pakyong, Sikkim, India © Springer Nature Singapore Pte Ltd. 2020 M. K. Solanki et al. (eds.), Phytobiomes: Current Insights and Future Vistas, https://doi.org/10.1007/978-981-15-3151-4_1

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known as mycorrhizae; the roots provide the fungi energy in the form of carbon, while the fungi provide the plant with often-limiting nutrients such as phosphorus. Besides, some soil microbiomes play a crucial role in the solubilizing stable form of potassium and micronutrients by releasing some metabolites which act as chelating agents. We explain recent information and cracks in these areas using phytobiomes. Keywords

Phytobiome · Soil fertility · Nutrient cycling · Soil organic matter · Soil health

1.1

Introduction

Developing countries like India need to produce a double quantity of foods to feed the population of the nation as well as the global crowds, whereas population growth touches 1.1% or 83 million annually. Feeding is not only mean full stomachs, but it mainly focused on nutritional security. The overall impact of rising demand for food production will depend on improved  productivity via high-yielding varieties and sustainable use of bioenergy (FAO 2017), whereas these higher yields of agricultural crops are vigorously influenced by regular nutrient accessibility and higher soil quality for promoting plant growth. Hence, there is an excellent chance of input-output imbalance, meticulous use of chemicals, organic matter depletion, removal of nutrients, and massive exhaustion of soil system through the anthropogenic activity for sustainable food production (Godfray et al. 2010). A sustainable food production system, which delivers both adequate nutrition and appropriate energy to people in the society, also improves the natural environment inter-­ generationally. To maximize the sustainability of production, we require a good strategic plan, which would help to acquire knowledge regarding components that may establish and sustain a healthy, productive agroecosystem. Integration and incorporation of this information into the present crop production system may further increase the total coverage of existing farmlands (mostly rehabilitated from degraded and marginal lands). Hence, to achieve the food and nutritional security with limited increased lands, we should first concentrate the interactions among the components of phytobiomes. The word “phytobiome” comprises phyto (plants) and biome (ecological area), which are very specific for plants and their surroundings. It includes plant interaction biology with sounding environments and living and nonliving objects (Leach et  al. 2017). Living entities include microorganisms, macroorganisms, and other plants and animals, and nonliving entities include soil, air, and climate. Simply, we can explain phytobiome as a conjoint venture of the rhizosphere, phyllosphere, biosphere, spermosphere, hyphasphere/mycorrhizosphere, and detritusphere (Nelson 2004; Frey-Klett et al. 2007; Vorholt 2012; Hacquard et al. 2015; Leach et al. 2017). Thus it is easy to say that phytobiome includes all entities that have a direct and indirect influence on plants and vice versa (Beans 2017). Phytobiome extends

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beyond the plant microbiome and unites facets including crop improvement and production, weather data modeling and forecasting, pest pollinators and pathogens, and data generation along with dissemination (Fig.  1.1). Moreover, phytobiome considers animals, pests, physical environment, management, and other pillars of sustainable agroecosystem that boost our scientific understandings and analytical aspects about plant microbiome also leveraging the computational power of “omics” (Young and Kinkel 2017). Spanning from fundamental to applied research aspects, researcher associated with phytobiome cover the areas of biotechnology, genetics-­ breeding, seed technology, agronomy, soil fertility and fertilizers, microbiology, plant pathology, nematology, entomology, meteorology, crop physiology, economics, statistics, extension, and more branches of agriculture (Fig.  1.1, Young and

Fig. 1.1  Phytobiome components and their interrelationship with different branches of agriculture. (Conceptualized and modified from Phytobiomes: A Roadmap for Research and Translation 2016; Young and Kinkel 2017)

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Kinkel 2017). However, composition, characteristics, and functions of healthy phytobiome, principally soil-plant-microbe interaction, are yet to be understood entirely.

1.2

Plant-Soil-Microbe Interactions in a Typical Phytobiome

In a typical phytobiome, phyllosphere gets more affected from the discontinuity of weather abnormalities (diurnal cycle), leaf surface, plant metabolism, environmental conditions (rain, wind, direct sunlight, and UV radiation), and nutrient availability (oligotrophic) than the rhizosphere (Leveau and Lindow 2001; Miller et al. 2001; Remus-Emsermann et al. 2012). Phyllosphere is a partial environment as compared to rhizosphere (Vorholt 2012). Though phyllosphere is also an essential aspect in the phytobiome study, nutrient cycling and soil health are controlled by the rhizosphere. Accordingly, we would like to concentrate on rhizosphere and rhizospheric engineering associated with plant nutrition and soil health. Discussion on soil-plant-­ microbe interaction in the rhizosphere can provide information regarding the influence of phytobiome on soil health, soil fertility, nutrient dynamics, as well as crop productivity. This rhizosphere is mainly crammed with plant roots having a significant impact on microbial composition and diversity as well as their activities (Andersen and Winding 2004; de Vries and Shade 2013). These organisms constituted with macrofauna like earthworms, ant, and termite; mesofauna like collembolan and acari; microfauna like nematodes and protists; macroflora like plant roots; and microflora like bacteria, fungi, actinomycetes, and algae (Coyne 1999; Mendes et al. 2013; Sarkar et al. 2017a). The further rhizosphere is differentiated into the endorhizosphere (mucoid layer coated root) and ectorhizosphere (rhizosphere soil). The community of soil microbes is so diverse than any other group of organisms that we are still able to explore very little diversity of genetic resources. Starting from decomposition, mineralization, or immobilization and subsequent humification in soil system up to plant growth and the functions of diversified microbial communities are affected mainly by management practices (Kennedy and Stubbs 2006). Nevertheless, soil respiration, microbial population, biomass, and enzymatic activities are significantly influenced by soil properties like pH, redox potential (Eh), clay mineralogy, soil organic matter content, and other nutrient levels (Sessitsch et al. 2001). In the humid subtropical mountainous ecosystems of India, urease activity was higher in the grassland ecosystem, whereas microbial population, dehydrogenase activity, and nutrient status were higher at Sacred Orchard (Arunachalam et al. 1999). While focused on soil structure, literature demonstrated that microbial biomass was the utmost concerted in silt and clay-sized soil particles, especially in silt and clay particle-associated micropores (5–30 mm) (Hassink et al. 1993a; van Gestel et al. 1996; Kandeler et al. 2000). Additionally, invertase, urease, and alkaline phosphatase activities were reported to be highest in the silty and clayey type of soil. Xylanase activity, which is considered to be the indicator of fungal activity (Kandeler et  al. 2000), was found to be higher in sand particles (Stemmer et al. 1998a, b; Kandeler et al. 1999; Kirchmann and Gerzabek 1999).

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Fig. 1.2  Nutrient cycling and interconnectivity of the atmosphere, lithosphere, biosphere, pedosphere, hydrosphere, and anthrosphere in a typical phytobiome 1 photosynthesis; 2respiration; 3gaseous exchange; 4deposition; 5weathering; 6decomposition; 7erosion; 8infiltration; 9percolation; 1leaching; 11capillary rise; 12manual application; red dashed arrow, immobilization; red solid arrow, mineralization

Though the population of fungi is much lower in grassland soil and arable fields, but its crucial role in the initial fragmentation of soil organic matter could not be ignored (Brussaard et al. 1990; Hassink et al. 1993b). Nutrient cycling and interconnectivity of the atmosphere, lithosphere, biosphere, pedosphere, hydrosphere, and anthrosphere in a typical phytobiome are represented in Fig. 1.2.

1.3

Beneficial Rhizospheric Microbes and Phytobiome

Rhizospheric microbes have an immense potential in sustainable, cutting-edge crop production. Furthermore, beneficial rhizospheric microbes (BRMs) are obligatory in biogeochemical nutrient cycles that drive soil fertility and crop productivity for the span of decades (Sarkar et al. 2017a). In general, these BRMs enhance the soil and plant productivity by means of (a) secreting hormones and other regulatory growth chemicals, (b) acquisition and bioavailable felicitation of essential nutrient elements, (c) inhibition of pathogens through biocontrol agent production, and (d) abiotic stress tolerance (Yang et al. 2009).

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A better understanding of environmental stress and its bio-modulation has also been possible with PBRMs (Schrey and Tarkka 2008; Ryan et al. 2009). Symbiotic association of rice and arbuscular mycorrhizae shrinks the drought stress effects by producing an antioxidative response and photosynthetic efficiency (Ruiz-Sanchez et al. 2010). Even though PBRMs and other rhizospheric microbes are insignificant in size, their population and activity are so significant that they are also considered as “dinner in the dark: illuminating drivers of soil organic matter decomposition” (van der Waals and de Boer 2017). Rhizospheric and non-rhizospheric microbes interact with each other either synergistically or antagonistically and are possible to change microbial community structure through differential soil, plant growth stages, feeding behavior on other taxa, acidity, reducing prey abundance, etc. (de Vries and Shade 2013; Leach et al. 2017). Preferential feeding like predation of gram-negative bacteria by protozoa (Andersen and Winding 2004) and predation over harmful bacteria by nematode may change the bacterial community. Interestingly, some Pseudomonas sp. could be able to prevent protozoan predation by producing antibiotics. The microbial collaborations and their network are recognized and synchronized but sometimes passive, through the fabrication and sensitivity of somatic and biochemical signals (Leach et al. 2017).

1.4

Phytobiome and Nutrient Stewardship in Soil

Though plants exclusively utilize inorganic forms of nutrients, soil organic matter (SOM) plays the “key to soil fertility” and nutrient dynamics in every soil systems, because SOM is the source for almost every essential plant nutrients. The content of SOM is considered as the indicator soil quality, microbial activity, and buffering capacity of the soil. Correspondingly, SOM could also be regarded as a critical element of phytobiome. Along with SOM dynamics, soil structure and nutrient cycling in the soil are greatly influenced by microbial processes, which are frequently affected by management (Kennedy and Stubbs 2006).

1.4.1 C-Cycle and Phytobiome Natural and agricultural-based soils are the significant source and sink for the dynamic flow of atmospheric CO2 as a result of the soil microbe-derived respiratory flux of CO2. Hence, concentrations of atmospheric CO2 are more sensitive to minute changes in the soil carbon cycle. Higher plants utilized atmospheric CO2 for photosynthesis, whereas microbes play the key role to maintain the source-sink relationship of SOC by altering the mechanisms involved in plant symbionts, detritivores, and phytopathogens. Moreover, preserve soil C by their death cells and plant roots (Amato and Ladd 1992; Lal 2004; King 2011). It has been reported that land use and management system influence soil ecosystems with the proliferation of microbial diversity which favor sequestration of C in soil (Singh et  al. 2010). So, here we will discuss

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microorganisms responsible in the global carbon cycle as well as climate change. This detail is required to maintain practical management of the soil-­plant continuum to nourish the microbes for stimulating soil carbon storage in agricultural soil.

1.4.1.1 Endurance of Soil Organic Matter and Its Microbial Decomposition The input of organic matter into the soil system is followed by two ways: (a) aboveground plant litter, crop residue, and organic manure including soluble organic carbon which penetrate into the soil with irrigation water and rainfall and (b) belowground roots and its rhizodeposition. Rhizodepositions often consist of simple organic compounds like carbohydrates, amino acids, organic acids, alcohols, etc. Perhaps with time rhizodeposition becomes humidified, which contains complex compounds like cellulose, hemicellulose, lignin, etc. (Wallenstein and Weintraub 2008). Mycorrhizal fungi play a vigorous role in the denaturation of the humified polymer. This mycorrhizal symbiosis seems to be found in approx. 85% of all plant communities usually in herbaceous crop (Smith and Read 2008). An experimental study shows that fungal partners are satisfied with the shifting of 20% (Nakano-Hylander and Olsson 2007) or even 30% (Drigo et al. 2010) of total assimilated carbon by plants having intense effects on rhizodeposition. A fraction of the plant carbon that is moved to the mycelia is rapidly respired back to the atmosphere, which results in a crack in the soil carbon cycle. A large portion of biomass is decomposed by heterotrophic microbial respiration causing loss of soil C. In addition, a small amount of the original C is reserved in the soil through the formation of stable organic carbon (Reynaldo et  al. 2012) that results in increased SOC stocks through C sequestration over time. The main microbial modulators for soil C storage are fungi and bacteria. The fungal/bacterial ratio is closely related with C sequestration potential in soils with more massive fungal abundance being correlated with higher C stock. Greater storage of C in fungal-­ dominated soils can be endorsed to improved C use efficiency, more extended protection of C in living biomass, and recalcitrant portion resulting in longer resident time of C.  Nevertheless, these observations are only relative, and it is still questioned whether fungal communities support soil C storage or whether soil with higher organic C favors soil fungi. Moreover, it can also be debated that fungi can negatively affect C storage due to their higher efficacy to decay recalcitrant litter (Cheng et al. 2012). 1.4.1.2 Microbial Functions in Soil Carbon Cycle Subsequent Climate Change Responses of climate change through carbon cycle are tangled because of microbial aids, their individual effects, and collaborations with other factors (Bardgett et al. 2008; Singh et al. 2010). A simple example of response to global warming is microbial activity, organic carbon decomposition, and CO2 release, which may be hastened in response to an increase in temperature (Davidson and Janssens 2006). This is further established by field observations that confirmed the positive correlation between higher respiration rates and elevated temperature regimes. Besides, a sign

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of secondary positive feedback to raise CO2 is a result of the photosynthetic production of carbon fertilization, whereas increased atmospheric CO2 accelerates photosynthesis (Bond-Lamberty and Thomson 2010) and the release of root exudates; consequently more labile carbon will be available for microbial decomposition and respiration. Readily available exudates after increased root deposition may “prime” the turnover of a passive pool of SOM that otherwise would not be subject to decomposition (Koyama et al. 2018). This difficulty is intensified by the diversity of soil ecosystems across the globe, which varies in their function due to their differences in forming factors including climate, organisms, relief, parent material, and time. Main interests on microbial activity in carbon cycle have been raised in peaty and frozen soils, where climatic conditions are not predicted for the addition or conservation of organic material, which may not be in favor of future climate, eventually in the release of sufficient quantities of CO2 to the atmosphere (Srivastava et  al. 2017). Further research in this area is very crucial if we can calculate the impacts and feedbacks between climate change and microbial function.

1.4.1.3 Microbial Growth Dynamics and Energy Balance Chemotrophic soil microbes fix soil C and N by synthesizing new biomass (Sokatch 1969; Dawson 1974). The energy balance and consequent thermodynamics equations are listed subsequently (adapted from Chen et al. 2003):  X Gr  Gs (1.1) where ΔGr is the energy released during respiration, ΔGs is the energy carrier (e.g., ATP) required to synthesized biomass, ε is the coefficient of energy transfer from ATP, and X is the balanced ratio of ΔGr (ATP used) and ΔGs (microorganisms involved). Stoichiometric yield coefficient (Y, biomass formed the unit amount of C or inorganic ingredients consumed (Dawson 1974; Chen et  al. 2003)) is calculated as follows: Y

  1  X 

(1.2) where α is the biomass (mg) formed from unit kcal energy consumption and β is the mass of organic and inorganic substances (mg) used to produce unit kcal energy:

 max  Yk (1.3) k



Y  max

(1.4)

where γmax is the maximum specific microbial growth rate (h−1 mg−1 biomass) and k is the maximum specific substance utilization rate (mg mg−1 biomass h−1) when ignoring microbial decay or maintenance. The rate of respiration, i.e., energy-­ yielding reactions, is constant and varying between 0.5 and 2.0 mg−1 biomass h−1 in many heterotrophs, autotrophs, aerobes, and anaerobes.

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From this declaration, the maximum specific substance utilization rate (k) and the maximum specific microbial growth rate (γmax) are expressed as Eqs. 1.5 and 1.6, respectively:



k

  0.5  2.0  1  X 

 max 

X

 0.5  2.0   X





(1.5) (1.6)

From Eq. 1.6, it is clear that both energy sources and microorganisms determine the maximum specific microbial growth rate (γmax). Thus, microbial growth in soil is dependent upon the types and diversity of microbes, and SOM content is described by Monod’s equation (Sokatch 1969; Dawson 1974; Chen et al. 2003):

   max

S  Ks  S 

(1.7) where S represents limiting nutrient (mg g−1), γ represents the specific growth rate (h−1  mg−1 biomass), and Ks is the half-velocity constant (Michaelis-Menten constant). Ks reproduces the affinity of the microorganisms for the growth-limiting nutrient and governs how quick the specific growth rate can reach the maximum rate and for efficient microbial work (Ks should be kept as small as possible). The Contois equation designates heterotrophic microbial growth; Eqs. 1.8 and 1.9 represent the dynamics of SOM depletion and biomass formation:



dA  max SA   kdA dt Ks  S

(1.8) (1.9)



dS 1   max SA     kdA  dt Y  Ks  S 

where A is the biomass (mg g−1) and kd is the specific microbial decay rate (h−1 mg−1 biomass). Complete understanding of the terrestrial microbial association and particular processes that govern the degree and fate of C dynamics will increase the prospect of successful management of the terrestrial ecosystem for increasing the stable C reservoir.

1.4.2 N Cycle and Phytobiome Nitrogen (N) is an essential nutrient required by plants for their growth and metabolism. The rate of N inputs in the agricultural system has doubled during the last century, potentially affecting both terrestrial and aquatic ecosystems. Even after excess application, it is often misplaced through volatilization, denitrification, or leaching and causes to limit its availability in most of the cultivated soils.

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1.4.2.1 Nitrogen Fixation and Transformations Although N abundantly exists in the atmosphere, the diatomic (N2) molecule is a comparative inert. Thus, N fixation by reducing the inert N2 molecule into NH3 is a complex process with the expense of an enormous amount of energy (Postgate 1982). Soil N stock and its variation depend on N transformation based on microbial dynamics and environmental conditions. The N transformation is mainly controlled by soil and residue C/N ratio (Chen et al. 2003). Other than C/N ratio, soil texture, pH, fertilizer quantity, crop rotation, soil and air temperature, soil moisture, and rainfall are some of the controlling factors of N transformation and stock variations (Nave et  al. 2009; Schipper and Sparling 2011). The diazotrophic microbes, which belong to the prokaryotic groups, fix atmospheric N2 with their normal metabolic process (Galloway et al. 2008). Some of these microbes are freeliving in the soil like Cyanobacteria, Proteobacteria, Archaea, and Firmicutes (Reed et al. 2011). Other organisms, including Azotobacter and Azoarcus genera, are also present at equivalent densities in the rhizosphere and non-rhizosphere soil. Bacterial genera like Herbaspirillum and Azospirillum colonize only in the higher plants’ rhizosphere (Mrkovacki and Milic 2001). On the other hand, some symbionts like Rhizobia are capable of infecting the root and form root nodules. Interestingly, this symbiosis has often limited to legumes. Thus, N fixation related to Rhizobium sp. has become a more exciting issue for researchers to unveil these complex environmental phenomena. A higher impact on primary productivity and economic feasibility is also one of the pillars for a sustainable agricultural ecosystem. Bacterial N fixation is a complex microbial process, where enzyme complex called nitrogenase (dinitrogenase reductase and dinitrogenase metal cofactor) takes part in the electron transport chain: the former enzyme serves as an electron donor, and the latter (substrate reduction component) accepts the energy of the electron to convert N2 to NH3. To generate one mole of NH3, 16 moles of adenosine triphosphate (ATP) is required, which are obtained from the oxidation of organic molecules. The N cycle and its processes are dynamic and simultaneously proceed to maintain equilibrium to nature. A diverse pool of nitrogenous compounds including organics (proteins, urea, amines, etc.) and inorganics (NH4+ and NO3−) in soil along with gaseous forms like NO and NH3 in troposphere determines N dynamics and bioavailability to the plants. Other than this, nitrification that is controlled by nitrifying bacteria includes nitrifiers (oxidizing ammonia to nitrite) and nitratifiers (oxidizing nitrite to nitrate). There are five common species of nitrifiers, Nitrosomonas europaea, Nitrospira briensis, Nitrosococcus nitrous, Nitrosococcus oceani, and Nitrosolobus multiformis, and three nitrifiers, Nitrobacter winogradskyi, Nitrospina gracilis, and Nitrococcus mobilis. Denitrifying microorganisms include Thiobacillus denitrificans and Micrococcus denitrificans and some species of Serratia, Pseudomonas, and Achromobacter (Delgado and Follett 2002). 1.4.2.2 N in Soil and Its Mineralization Being the most extensively limiting plant nutrient in agriculture, fertilizer N is the main depending material for half of the global population for their daily

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hand-to-­mouth activities. Total N content varies from 0.02% to 0.44% across the globe, the tropical country like India lacks SOM, causing consequently low soil N in surface soil layers. In India the total N content of surface soil ranges from 0.02% to 0.13%  (Motsara 2002). Whether in the forest cover or the agricultural fields, crop-­covered soils result in 10–20 times higher soil N content than the open fallow lands. Excessive cultivation leads to disintegration and decomposition of SOM, which leads to a decrease in N content in soils. Studies have shown that up to 3.5% of organic N in soil is mineralized annually. Even this rate of mineralization can take care of the normal growth of plants, except under sandy soils with inferior organic N; also crop demand of N is more than the mineralization rate (Chen et al. 2003). In a sandy loam soil, a 50% combination of sewage sludge and fertilizer could be one of the possible and best alternatives to curb fertilizer N and enhance N use efficiency (Biswas et al. 2017). As of advances in technology, the N stable isotope (15N) technique has been widely used as a measuring tool in ecological studies of N cycling. This because of 15N natural abundance values (δ15N) of soil samples is the net result of many biogeochemical processes that can cause 15N refinement (Frank et al. 2000; Ghosh et al. 2018).

1.4.3 Phosphorus Nutrition and Phytobiome Phosphorus (P) is one of the major nutrients essential to sustain all forms of life and is indispensable for the functioning of virtually every living cell on this planet. It is essential for energy metabolism and the principal component of adenosine diphosphate (ADP) and adenosine triphosphate (ATP). It is an important constituent of the genetic components deoxyribonucleic acid (DNA) and ribonucleic acid (RNA), and plays an important role in almost all metabolic processes in plants. An adequate amount of P is essential for root development, growth, and maturity of all the crop plants. It is second only to nitrogen (N) in terms of its limiting nature to plant growth, in almost all arable soils across the globe.

1.4.3.1 Phytobiomes and P Nutrition in Plants The complex chemistry of P and its widespread deficiency in the world soils have driven the plant community to develop and adopt several strategies to improve the acquisition of P from marginally P-deficient soils. Changes in the root configuration, morphology, and distribution (de Souza et al. 2016), production of different organic compounds by the roots which helps in dissolution of inorganic P compounds in soil, and alliance of the plant roots with beneficial microorganisms in the rhizosphere (Zhou et al. 1992; Hasan 1996; Sharma et al. 2007) are some of the unique strategies adopted by the plants to strive over P-deficient situations. It is estimated that the amount of P fixed in world soils would be able to sustain crop production for the next 100  years if properly mined using available techniques (Goldstein et al. 1993).

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1.4.3.2 Microbiome and P Nutrition in Plants The phosphate-solubilizing microorganisms (PSMs) are essential for P nutrition of plants, and in the soil, the population of phosphate-solubilizing bacteria is higher by 2–50-fold compared to fungi. However, the fungal isolates in both solid and liquid culture media exhibited higher P-solubilization capacity compared to bacteria (Gaur et al. 1973; Banik and Dey 1982; Kucey 1983; Harrison 1987; Kucey et al. 1989). Of the various P compounds present in the soil, the Ca-P is more readily solubilized by the PSMs, while very few are reported to solubilize the Fe and Al-P which are the major compounds in acid soils like alfisols (Fig. 1.3). The PSMs are very effective in insolubilization of rock phosphates (RP) which are generally Ca-apatites and increase the P availability to crops when applied along with rock phosphates in soil. Currently, different species of bacteria such as Azotobacter chroococcum, Bacillus subtilis, Bacillus cereus, Bacillus megaterium, Arthrobacter ilicis, Escherichia coli, Pantoea agglomerans, Pseudomonas putida, Pseudomonas aeruginosa, Enterobacter aerogenes, Microbacterium laevaniformans, and Micrococcus luteus have been identified as effective P solubilizers (Kumar et al. 2014). The microbial association thus plays a significant role in P nutrition particularly in the low P soils, and often the level of soil P determines the nature of microbes that get associated with plant roots (Gomes et al. 2018). Different maize genotypes with variable P acquisition capacity had a different association with microorganisms, and the P levels in the soil primarily guided this. The slow-growing microorganisms were more abundant in soil with low P levels, while the fast-growing

Fig. 1.3  Different fractions of soil P based on sources and chemical properties

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microorganisms were predominant in the soils with high P levels (Gomes et  al. 2018). In general, several bacterial species like the Pseudomonas, Enterobacter, Azotobacter, Burkholderia, Rhizobium, etc. are associated with P-solubilization and promote plant growth (Oliveira et al. 2009; Glick 2015; de Souza et al. 2016; Alori et al. 2017). However, the population of phosphate-solubilizing organisms was not affected by the level of P in soils (Browne et al. 2009; Gomes et al. 2018; Robbins et al. 2018). Besides the P-solubilizing bacteria, the arbuscular mycorrhizal fungi (AMF) play an essential role in the P nutrition of plants. The hypha of the AMF acts as an extension to the plant roots and helps in exploring more soil volume, increasing the P availability to plants, and acting as an unhindered pathway for translocation of P (Schweiger and Jakobsen 1999). However, the soil P level is again critical, which regulates the abundance of AMF association with plant roots. Low soil P level increases the AMF association with plant roots, while P fertilization harms the AMF establishment. The AMF colonization in maize reduced from 29.2% to 13.7% when the soil P concentration was raised from 15 ppm to 70 ppm (Gosling et al. 2013). The plant species is an essential factor determining the association of AMF, and it is higher for crops like maize, cotton, pigeon pea, sunflower, mung bean, and sorghum while lower for oats, wheat, barley, etc. (Seymour 2009). Sometimes even the non-P-solubilizing microbes play an essential role in P nutrition. These organisms take up sparingly soluble P compounds from the soil with the help of high-affinity P transporters, which becomes available to plants upon the death of the microbes (Gyaneshwar et  al. 2002). The extremely insoluble P compounds are also cycled and become available for plant nutrition. Escherichia coli, a non-P solubilizer helps in the P nutrition of plants (Wanner 1996). Under P-limiting situations, the P transporters in Rhizobium are activated, resulting in higher accumulation of P and enhanced alkaline phosphatase activity (Al-Niemi et al. 1997).

1.4.3.3 Rhizosphere Engineering and P Nutrition Root-induced changes in the rhizosphere also help in P acquisition and improve the P availability to plants (Hinsinger 2001). The plant root secretes a large number of substances that alter either the soil pH or chelating substances which are capable of releasing P from sparingly soluble P compounds. The secretion of organic acid molecules like citrate, oxalate, etc. also helps in P release through ligand exchange and increases P availability to plants (Shen et  al. 2011). The plant roots also secrete enzymes like phosphatase or phytase, which can mobilize the organic P from the soil and make it phyto-available (Neumann and Romheld 2002; Zhang et al. 2010). Some of the new hypotheses are postulated based on the PSM-inspired chemistry by deriving polymer-coated P fertilizers to enhance PUE (Sarkar et al. 2017b; Sarkar et  al. 2018). Also, nano-formulation of natural resources like phosphate rock increases the specific surface area that helped in better microbial activity and further improved PUE with or without organic acids (Roy et al. 2015, 2018a, b).

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1.4.4 K-Bioavailability and Phytobiome For achieving sustainable crop productivity, nutrients are the necessary inputs, and potassium is one of them. The flaws between depletion and the use of K fertilizers in agriculture are flaring day by day. So, it is relative to know the potassium dynamics in soil corresponding with potassium needed for the crops which offer balanced nutrition and retain its status in soils. Addressing this nutrient inequity and deficiencies, increased manufacture of potassium fertilizer is necessary for India and other developing countries. In these situations, it is required to prosper natural mineral sources of K to replace costly fertilizers. Although these minerals are not readily soluble, the combination of potassium minerals with a potassium-solubilizing microorganism (KSM) would be a better and available knowledge to increase bioavailability of K from K-bearing minerals, which could help in maintaining the ecological balance and sustaining agricultural production and environmental quality. Now, the question is how these soil organisms solubilize K.  The processes involved in K solubilization are listed and described in the following (Fig. 1.4).

1.4.4.1 K-Solubilizing Microbial Species Soil presents a variety of microbiomes including bacteria and fungi which boost the solubility of K minerals through the production of organic synthetics including chelating agents, exudates, extracellular enzymes, metabolic by-products, and both simple and compound organic acids (Meena et al. 2014; Saha et al. 2016a, b). These enzymes and organic metabolites triggered the biotic weathering of K-bearing rocks

Fig. 1.4  Mechanisms of K solubilization in a typical phytobiome. (Conceptualized and modified from Meena et al. 2014; Saha et al. 2016a, b)

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and minerals. Especially rhizobacteria produce 2-keto-L-gluconic acid which binds Ca and acts as a strong weathering factor for underlying rocks. Otherwise, soil microorganisms respire and produce CO2 that reacts with water and forms carbonic acid. This carbonic acid contributes to chemical weathering by dissolving CaCO3 and K minerals through dissolution reactions. Negatively charged soil particles adsorb maximum cationic nutrients like K and retard bioavailability. However, acidification of soil by the soil microbiomes assists in ion exchange processes. In this way, K is released into the soil solution and becomes readily available to the plants. Similar charge species are also involved in ion exchange when their presence is higher in the soil solution. For example, when Ca2+ is present in excess in the soil solution, it can exchange two K+ ions from the soil adsorption sites and contributes to desorption and K solubilization. These ions also transfer K, which is trapped in the interlayer spaces of the minerals to some extent. Certain bacteria produce mucilage like extracellular polysaccharides (ESP) which form a wrapper around the bacterial cell, attack the clay minerals chelating with silicon, and consequently release K from that structure. Fungi are also considered as a biological weathering referee of rocks, minerals, and building blocks. Ectomycorrhizal hearting networks and the arbuscular structure of non-ectomycorrhizal trees, embedded in biofilms, conduct nutrients to the host. Here, biofilms assist in stimulating the weathering of minerals and thereby increasing uptake of nutrients to the plant. Some rock-decaying fungi can ooze out organic ions having low molecular weight, which forms a microscopic tunnel in the vicinity of exudates at hyphal tips within the minerals which enhances the weathering rates in that soil. This is supported by numerous studies, whereas a wide variety of bacteria like B. mucilaginous, B. edaphicus, B. circulans, Burkholderia, Acidithiobacillus ferrooxidans, Paenibacillus spp., and Pseudomonas spp. have been demonstrated to solubilize K from K-containing minerals in the soils (Liu et al. 2012; Meena et al. 2014). Zhang and Kong (2014) isolated and identified that strains of Pantoea agglomerans, Agrobacterium tumefaciens, Microbacterium foliorum, Myroides odoratimimus, Burkholderia cepacia, Enterobacter aerogenes, E. cloacae, and E. asburiae remain effective in K solubilization in both solid and liquid media. Several other studies also validated the significant role of plant growth-promoting rhizobacteria (PGPR) in K solubilization and its mobilization in the plant root systems (Kumar and Singh 2001; Kukreja et al. 2004; El-Fattah et al. 2013).

1.4.5 S Cycle and Phytobiome Sulfur (S) containing amino acids (cysteine, cystine, and methionine) is present in almost all the proteins, which makes it indispensable to more or less all living organisms. These amino acids may be present as free or in combined states. S cycle includes the transformation of S from organic to inorganic or inorganic to organic form and oxidized state to reduced state or reduced to oxidized state. These processes are mediated by various microorganisms, especially bacteria (Schoenau and Malhi 2008).

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1.4.5.1 Mineralization and Immobilization of Sulfur Sulfur mineralization is the conversion of plant-unavailable organically bound forms of sulfur (organic sulfates and carbon-bonded sulfur) to the plant-available inorganic forms of S (sulfate, SO42−) in soil. Whereas immobilization is exactly the opposite process, where inorganic S is assimilated by living organisms (microbes) and converted to the organic forms, that plant cannot absorb. In unfertilized soil S mineralization is the dominant source of S, in S pool for plants throughout the year (Bettany et al. 1979). The main factor which decides whether an organic S source will be mineralized or immobilized is the C/S ratio. When the C/S ratio is less than 200:1, net mineralization occurs, and organic S contributes to plant-available pool of S; in case the C/S ratio of the organic matter exceeds 400:1, net S immobilization occurs, and plant-available S is converted to organic S (Schoenau and Davis 2006). Organic S consists of (1) organic sulfate (S and C are not directly bonded like thioglucosides, sulfate esters, and sulfamates; here S is bonded to C via oxygen or nitrogen) and (2) carbon-bonded sulfur (here S is directly bonded to C like sulfonic acids, sulfur-containing amino acids in proteins). Organic sulfates cover 30–70% of the total soil organic S. S-containing amino acids and organic sulfates are the labile forms of organic S; they mineralize very easily by extracellular enzyme arylsulfatases (Tabatabai and Bremner 1970). Through organic mineralization, S is converted to sulfate (SO4−2) and thiosulfate (S2O3−2) which are absorbable by plants. Humus soil has a C/S ratio nearly 100:1. Thus decomposition of it results in net mineralization (Roberts et al. 1989). 1.4.5.2 Microbial Oxidation and Reduction of S Soils where reduced forms of S (such as sulfides, elemental sulfur) are present, in those places microbial oxidation of reduced inorganic S is an important process. Through oxidation, reduced (–2, 0) forms of S (S2−, S0) are converted to higher oxidation states (+6) like sulfate (SO42−). Both autotrophic and heterotrophic microorganisms perform microbial oxidation, including species of Thiobacillus (autotroph); heterotrophic bacteria like Bacillus, Arthrobacter, and Pseudomonas; and some fungi (Lawrence and Germida 1988). In some cases, heterotrophic sulfur oxidizers may dominate, especially in the rhizosphere (Grayston and Germida 1990). S oxidation is an acidifying process. It can be depicted by the following equation where elemental S, a reduced form of S, is oxidized to sulfuric acid:

2 S0  3 O2  2H 2 O  2 H 2 SO 4

As a result of flooding, reduced aeration and high oxygen consumption produce reducing conditions, where redox potential decreases and drives the microbial conversion of sulfates to sulfide after other electron acceptors including oxygen and nitrate are depleted. This is termed as dissimilatory sulfate reduction, which is performed by the species of Desulfovibrio and Desulfotomaculum bacteria. Hydrogen sulfide gas is retained in the soil by reaction with iron to form an iron sulfide mineral, depicted in the following equation:

SO 4  H 2 S  g   Fe  FeS  mineral 

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These sulfides may be oxidized back to sulfates if the soil becomes aerobic again (Schoenau and Malhi 2008).

1.4.6 Trace Metals and Phytobiome The huge quantity of effluents generated from households and industries is continuously contaminating the land, river, pond, as well as groundwater aquifers (Saha et al. 2017a). Subsequent contamination of the human food chain from a significant amount of metals and pollutants is accumulated in soil following crop accumulation. As metals like iron (F)e, manganese (Mn), zinc (Zn), copper (Cu), and nickel (Ni) are essential for plant growth (Hapke 1991; Lenka et  al. 2016; Saha et  al. 2017b), apart their required quantity is significantly lesser than the N, P, and K. Thus, these metals along with other beneficial and harmful cationic metals are often defined as trace metals, whereas the term “heavy metal” is a cumulative term that includes both metals and metalloids having an atomic number of more than 20 (Ca) or atomic density more than 5 g cc−1 which also cause toxicity at very trace concentration. Moreover, trace metals like chromium (Cr), cadmium (Cd), cobalt (Co), selenium (Se), mercury (Hg), lead (Pb), and arsenic (As) are responsible for different types of malfunction or even death due to toxicity in plants as well as animals and adversely affect the soil system. However, the levels of toxicity are determined by the combination of different factors like soil pH, conductivity, and other ionic activities in soil solution and particular metal species (type) and concentration present in ecosystems (Tchounwou et al. 2012; Saha et al. 2017c). Metal toxicity induced poor plant growth, retarded carbohydrate and protein metabolism, obstructed growth hormone formations and enzyme activities, and simultaneously insisted reduced biological diversity in the rhizosphere and non-rhizospheric soils (Singh et al. 2011).

1.4.6.1 Conducive Soil Condition for Trace Metal Toxicity Certain conditions induce trace metal toxicity for crops and humans. These trace element toxicities occur in the following (Bucher and Schenk 2000; Broadley et al. 2007; Aref 2011): (a) Superfluous application of untreated sewage sludge, municipal waste, tannery and distillery effluents, coal combustion ashes, etc. (b) Light-textured soil with low pH and having impeded subsurface soil layer with very low hydraulic conductivity (c) Mineral soil having deficient soil organic matter (d) Intensive raw minerals (e.g., waste mica, rock phosphate, pyrite, etc.) and fertilizer application (e) Irrigation with polluted groundwater (f) Type and concentration of trace metals in the environment Heavy-trace metals are distributed over the solid phase, liquid phase, and also the gaseous phase, and their partitioning influenced and depends on complexation with

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ligands, ion exchange, adsorption-dissolution-precipitation reaction, and oxidation-­ reduction reaction (Vlek et  al. 1974; Singh and Saha 1997; Rattan et  al. 2008). These interacting properties are the controlling factors of trace metal solubility, mobility, and bioavailability in soil and water systems. Other than mechanical and chemical processes, microbial inoculation has the potentiality to reduce the metal toxicity by either decomposition or immobilizing the metals from the soil (Abou-­ Shanab et al. 2003; Seshadri et al. 2015).

1.4.6.2 Trace Metals’ Crop Response and Phytoremediation Negative interaction of cationic trace metals induces other trace metal deficiencies in plant tissues. Khan and Khan (2010) reported that Fe and Zn uptake was reduced from the excess application of Ni and developed chlorosis symptoms on leaves. Other reports also indicated that Cd toxicity induces poor Cr uptake (Dotaniya et al. 2017); and Zn toxicity induces Fe and Mn deficiency in plant tissues (Sivasankar et al. 2012). Correspondingly, specific metal toxicity also affects the dynamics of nutrient mineralization and nutrient release kinetics and results in poor plant growth; plants appeared brushy (Singh et al. 2016). Trace metals’ (heavy metal) toxicity also retard soil enzymatic activity by replacing the native essential metals from binding sites (Bruins et  al. 2000). For example, excess concentrations of Cd2+, Ag2+, and Hg2+ in the soil-solution exchange phase are likely to bind with SH groups of some sensitive enzymes, which retard the activity of the enzyme (Nies 1999). Thus, increasing the use of wastewater, municipal wastes, industrial effluents, and coal combustion ashes triggers the toxic trace metal concentration in soil, which further accelerates the metal accumulation in ecological habitats (Rajkumar et al. 2012). Apart from this, higher Cr concentration was reported in plant roots compared to shoot, because metal excluder plants can store an excessive amount of Cr in root cell vacuole (Oliveira 2012; Nematshahi et al. 2012). Contrastingly, untreated sewage sludge application enhances crop yield, soil nutrient content, organic C content, and soil biological activities (Roy et  al. 2019). Integrated approach (treated organic waste and inorganic fertilizers) is the best-recommended method for sustainable soil management and crop production. Neither the excess of essential nutrients nor other trace elements are beneficial for the plant-soil-microbe system, because specific element toxicity damages the DNA structure of soil enzymes and disturbs the normal functionality in the environment (Bruins et al. 2000). 1.4.6.3 Siderophore and Phytosiderophore Engineering and Trace Metal Chemistry Due to certain unwanted and challenging environmental conditions, the release rate of plant root exudates enhances the rhizosphere. These exudates help both ways by accelerating essential nutrient elements and inhibiting toxic elements (Marschner 1995). During Fe and Zn deficiency, graminaceous plants like barley, wheat, etc. exude phytosiderophores. While these exudates are produced from soil microbes, other higher plants are termed as siderophores. Siderophore and phytosiderophore are hexadentate non-proteinous amino acids, which act as a ligand and coordinate with Fe3+, Zn2+, or Mn2+ by the carboxylic and amino groups (Romheld 1991). In the

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rhizosphere, metal chelation is not specific for Fe3+. Subsequently, phytosiderophores can transport a wide range of metals like Zn, Cu, Mn, Cd, and Ni (Awad and Romheld 2000). The diurnal variation of phytosiderophore release is also specific with plants and parts of plant roots. Generally, maximum phytosiderophore release and microbial activity are observed near the apical root zones due to localized microbial degradation and distribution of phytosiderophore (Marschner et al. 1986; Romheld 1991). The rate of phytosiderophore (PS) release differs among interspecies, plant to plant, and depends on daytime, sunshine hours, light intensity, and micronutrient status (Cakmak et al. 1994). However, this correlation with phytosiderophore quantity is not always consistent. Siderophores and phytosiderophores associated with metal chemistry and metal bioavailability in the soil are listed in Table 1.1. In contrast with Zn-PS and Mn-PS, the preferential uptake of Fe-PS is more prominent, which is mainly regulated by soil Fe nutritional status. The affinity of mugineic acids (MA) for heavy metal cations decreases in the order of Cu2+ > Fe3+ > > Zn2+ > > Mn2+ (Dotaniya et al. 2014). Fe-PS and Zn-PS complex uptake rate corresponds to ~100 and ten times higher than that of free Fe and Zn. Thus, PS production and subsequent uptake are regulated by the transporters of the YS1/YSL protein family, which is induced by Fe deficiency (Meda et  al. 2007). Due to increased nutrient availability, this process is also considered as a lifesaving mechanism for plants.

1.5

Phytobiome: An Early Indicator of Soil Health

Typically, soil health is defined as “a state of dynamic equilibrium between flora and fauna and their surrounding soil environment in which all the metabolic activities of the former proceed optimally without any hindrance, stress or impedance from the letter” (Goswami and Rattan 1992). Simultaneously the soil quality, which is analogous to soil health, is often used in the scientific literature, as scientist prefers soil quality. Soil quality is defined as “the capacity of soil to function within the ecosystem and land-use boundaries, to sustain biological productivity, maintain environmental quality, and sustain plant, animal, and human health” (Doran and Parkin 1994). On the other hand, soil health is generally dealt with by the producers (e.g., farmers). There are few conceptual differences between soil quality and soil health, where the former considers soil usefulness for a particular purpose for a long time scale and the latter considers the state of soil for a particular time (Larson and Pierce 1991). Healthy soils are very crucial for the reliability of global ecosystems to stay integral or to recuperate from biotic and abiotic stresses as well as anthropogenic exploitation with agriculture (Ellert et al. 1997). In soil, phytobiome has the capacity to provide an integrated standard tool for soil health and quality, which cannot be obtained from physical or chemical analyses of soil. Microbiomes quickly acclimatize to environmental conditions as they have close relations with their surroundings due to their higher surface-to-volume ratio and respond rapidly to changes. Hence, the potentiality of these biomes can be adapted as an excellent indicator of soil health assessment. In some cases, alterations in microbial populations and activity

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Table 1.1  Siderophores and phytosiderophores associated with metal chemistry and metal bioavailability in soil Plants and microorganisms Plants Graminaceous family

Microorganisms Bacteria Bacillus Nocardia, Arthrobacter Escherichia coli Staphylococcus Erwinia chrysanthemi Mycobacterium tuberculosis Pseudomonas sp. Bordetella sp. Azotobacter, agrobacterium Arbuscular Cenococcum geophilum, mycorrhizae Wilcoxinarehmii Glomus etunicatum, G. mosseae, unidentified Glomus sp. Fungi Rhizopus Ustilagosphaerogena Fusarium roseum Neurospora crassa Aspergillus fumigants, Penicillium bilaiae Aspergillus ochraceus

Siderophore and phytosiderophore production Phytosiderophores: mugineic acid (MA), deoxymugineic acid (DMA), epoxy-mugineic acid (EMA), hydroxy-mugineic acid (HMA) Siderophores: Schizokinen, bacillibactin, ferrioxamines Ferrioxamines Enterobactin Staphyloferrin Chrysobactin, achromobactin Mycobactin Pyoverdines Alcaligin Catecholate Ferricrocin Glomuferrin

Rhizopherin Desferriferrichrome Fusarinines, malonichrome, triacetylfusarinines Ferricrocin Pistillarin Ferrichrome

Adopted and modified from Matzanke et al. (1988), Hider and Kong (2010), Dotaniya et al. (2014), Winkelmann (2017), Sarkar et al. (2017a, b), Hussein and Joo (2017)

before detecting changes in soil rather than physical and chemical properties thus provide an early signal of soil improvement or an early indication of soil degradation (Pankhurst et al. 1995). The turnover rate of microbial biomass is much faster (1–5  years) than the total soil organic matter turnover (Carter et  al. 1999). Phytobiomic indicators of soil health involve various sets of microbial dimensions due to the multifunctional characteristics of microbial groups in the terrestrial ecosystem. Some indicators of soil health are as follows: 1. Biodiversity: genetic diversity, functional diversity, structural diversity 2. Carbon cycling: soil respiration, organic matter decomposition, soil enzymes, methane oxidation 3. Nitrogen cycling: N-mineralization, nitrification, denitrification, N-fixation 4. Soil biomass: microbial biomass, protozoan biomass

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5. Microbial activity: bacterial DNA synthesis, bacterial protein synthesis, RNA measurements, bacteriophages 6. Bioavailability: biosensor bacteria, plasmid-containing bacteria, antibiotic-­ resistant bacteria, catabolic genes In addition to the influence on nutrient cycling, microbiomes also affect the physical properties of soil by producing extracellular polysaccharides and other cellular trashes that help in maintaining soil structure. As these biochemicals function as chelating agents, they stabilize soil aggregates and affect water retention capacity, crusting, erodibility, infiltration rate, as well as susceptibility to compaction.

1.6

Future Outlook

Attempts are to be made to enhance the food, feed, and fiber production worldwide by exploring each and individual component of phytobiome and in between interactions. Due to increased food demand and high-intensity agriculture, integration and optimization of phytobiome-based pieces of knowledge, resources, and siteand condition-specific solutions become one of the most treasured materials for sustainable agriculture and soil health. Further, an advanced association of scientific society to explore this concept is a much important future aspect of phytobiome studies.

1.7

Conclusions

This chapter is an effort to enlighten the idea of phytobiome and its role in nutrient regulation, maintaining soil quality. The modern principles of different utilizations of this phytobiome have been characterized to excerpt a high prospect of their functionality and applicability for sustainable agriculture. So, these phytobiomes are evolved as plant growth-promoting microbiomes, which are important for keeping good soil health, better soil conditions, and persistent agricultural productivity. These biomes do not become alive independently but make interconnected coordination with the environment. All are engaged in the nutrient cycle of the terrestrial ecosystem by weathering and solubilizing complex and stable nutrient sources. The contest of this section is to develop new approaches for addressing the nutrient use efficiency as well as directed plant parts (within metabolomes of rhizospheric groups) to assist a significant change in the level of perception. The ultimate aid from this section will be the information about modification of the soil-plant system to support microbial chemistry or their effects on soil physico-chemical properties that are most important in promoting nutrient acquisition in plants across the diversified global agricultural condition. These provide an effective substitute for advanced crop production.

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Role of a Quorum Sensing Signal Acyl-­ Homoserine Lactone in a Phytobiome Pushparani D. Philem, Avinash Vellore Sunder, and Sila Moirangthem

Abstract

A phytobiome is influenced by its many members, which includes plants, soils, microbes, animals (insects), and the constantly fluctuating environment. Plant-­ microbe interactions represent one of the most impactful relationships inside a phytobiome and may have a beneficial, harmful, or neutral effect on one another. This chapter provides a comprehensive analysis of the complex network of signal exchange between microbes and plant in a phytobiome, via the quorum-­sensing circuit with a special focus on N-acyl homoserine lactones (AHLs) signaling. Incorporating the current understanding of this plant-microbe dynamic by tracing their signals is one of the major tools to customize a sustainable phytobiome. There are still many gaps to cover such as understanding a system-level communication of the phytobiome and the molecular nitty-gritty of signal transport within plants and molecular pathways coordinating plant physiological changes. Future advances would depend on the collaborative effort of interdisciplinary scientist groups backed by advance “omic” techniques to link all the biotic and abiotic components and understand the synchronized dynamic of a phytobiome. Keywords

Phytobiome · Quorum sensing · N-Acyl homoserine lactones · Signaling · Microorganism

P. D. Philem (*) Biochemical Sciences Division, CSIR-National Chemical Laboratory, Pune, Maharastra, India A. V. Sunder Department of Chemical Engineering, IIT Bombay, Mumbai, Maharastra, India S. Moirangthem Tissue Culture Laboratory, Research Silviculture and Training Division, Imphal, Manipur, India © Springer Nature Singapore Pte Ltd. 2020 M. K. Solanki et al. (eds.), Phytobiomes: Current Insights and Future Vistas, https://doi.org/10.1007/978-981-15-3151-4_2

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Introduction

Given the ever-increasing food demand and energy crisis in the world today, increasing biomass yields for greater food supply and low-cost, low-maintenance energy crop production without the use of harmful synthetic agrochemicals is the need of the hour. In recent years, there has been a paradigm shift in the understanding of the nature of plant-associated community, from the perspective that a plant is strongly interconnected with different biotic factors such as plants, animals, and microorganisms and abiotic factors like soil, light, and water and that sustainable improvement in agro-productivity and agro-quality would require a system-level approach, taking into account all the optimum biotic and abiotic set of influences on a plant (Leach et al. 2017). Phytobiome is defined as the totality of a plant, its physical environment, and the entire population of microorganism in, on, and around the plant. The composition of biotic community associated with the plant depends on the host genotype, local niche, or the plant compartment (spermosphere, endosphere, rhizosphere, phyllosphere) and environment such as soil type (Hacquard et  al. 2015; Leach et al. 2017). For example, phyllosphere, the aerial plant part, experiences a highly fluctuating environment and nutrient availability and hosts a more distinct microbiome as compared to a more environmentally stable rhizosphere (Remus-­ Emsermann et al. 2012). Chemical communication plays a major role in the growth, development, and evolution of plants (Witzany 2006). For example, plants release volatile compounds to invite insects to help them spread their pollen for reproduction (Baldwin 2010). A good understanding of the integrity and the basic administration in a phytobiome would help to design strategies toward sustainable agriculture and environmental preservation. This would require a sound understanding of the communication among the various members of a phytobiome. However, since signals can be quite often co-opted, modified, or even destroyed by another member of the community, there is the need for a system-level analysis of communication within the phytobiome (Leach et al. 2017). Microbes represent the largest biotic component of a phytobiome, which also exist in the closest proximity, that is, on, around, and inside of a plant. Plants and microbes have co-evolved over time, interacting both in symbiosis and pathogenesis, and so has the communication signaling network between the two kingdoms (De-la-Peña and Loyola-Vargas 2014). The microbial world communicates via signaling molecules based on the population size-driven phenomenon of quorum sensing (QS) (Fuqua and Winans 1994). Bacterial QS machinery consists of an autoinducer, its cognate receptor protein, and a synthase gene for signal synthesis. QS-controlled bacterial phenotypes include bioluminescence, biofilm formation, motility, conjugation, sporulation, production of antibiotics, and the expression of virulence factors (Williams 2007). Disruption of the QS system or quorum quenching (QQ) takes place by (1) signal degradation by enzymes and physical agents, (2) inhibition of signal synthesis, and (3) receptor blocking (Uroz et al. 2009). Given this myriad of roles of QS in both pathogenic and symbiotic interaction, QS and QQ find multiple applications in agriculture and medicine (Grandclément et al. 2015).

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Common bacterial QS signal molecules, such as N-acyl homoserine lactones (AHLs), diffusible signal factors (DSF), and signaling peptides, are among the best-­ studied communication signals in the phytobiome (Leach et  al. 2017). AHLs produced by Gram-negative bacteria are the most reported autoinducer signal molecules. AHLs can be defined by the length of their acyl chain, with short-chain (C4-C6), medium-chain (C6-C10), and long-chain (C10-C16) AHLs. AHLs are produced by both pathogenic bacteria and plant growth-promoting rhizobacteria (PGPR). Table  2.1

Table 2.1  Different QS signaling molecules and their effect on plants along with the probable mechanism of action

QS molecule N-Acyl homoserine lactones (AHLs)

Aryl HSLs

Producers Gram-negative bacteria

Rhodopseudomonas RpaR, BraR palustris, Bradyrhizobium

Diffusible signal factor (DSF)

Stenotrophomonas maltophilia, Xanthomonas, Burkholderia cenocepacia, Pseudomonas aeruginosa Cyclodipeptides/ Pseudomonas diketopiperazines aeruginosa Autoinducing peptides (AIPs)

Probable mechanism of action LuxR receptor/G-­protein signaling Induction of salicylic acid and oxylipin-­ dependent pathways

Gram-positive bacteria

RpcF/RpfG two-­ component system

Auxin signal mimics Not known

Effect on plant Seed germination and plant development (C6HSL) Root elongation (3OC6HSL, 3OC8HSL) Primary root growth, lateral root formation, and root hair development Increased defense and systemic resistance against fungal pathogens “Priming” for induced resistance and rapid and robust response to abiotic stresses (C12HSL, OC14HSL) Not known

References Moshynets et al. (2019) Jin et al. (2012) Ortíz-Castro et al. (2008)

Promote plant growth, lateral root development

Ortiz-Castro et al. (2011)

Schuhegger et al. (2006) Schenk et al. (2014) and Schenk and Schikora (2015)

Schaefer et al. (2008) and Ahlgren et al. (2011) Alavi et al. Promotes seed germination and plant (2013) and Venturi and growth, enhanced Keel (2016) biocontrol, elicit innate immunity in plants

Monnet et al. (2016)

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provides a list of QS signal molecules reported for their effect on plants and possible mechanism of action. Many reports have shown that plants can detect and respond to AHLs, and the responses differ based on the acyl chain length and substitution of the AHL molecule and the plant species-AHL combination (Mathesius et  al. 2003; Schuhegger et al. 2006; Schikora et al. 2011; Schenk et al. 2014). This chapter summarizes the current knowledge of (a) how AHL signaling in a phytobiome impacts plants, b) how plants manipulate AHL signals to their advantage, c) the basic dynamic of the plant-microbe signal exchange, and finally d) how this knowledge can be incorporated in the bigger scheme of creating a healthier phytobiome.

2.2

Plant Senses and Responds to AHL

The first report on the impact of bacterial AHLs on plant physiology was a differential proteome analysis of M. truncatula roots, studying their response to the exposure of 3OC12-HSL and 3OC16:1-HSL, in nanomolar (nM) concentrations (Mathesius et al. 2003). This work revealed complex functional responses to AHL application in the plant, with significant changes in the expression of over 150 proteins. The proteins detected were associated with defense, stress responses, energetic and metabolic activities, transcriptional regulation, protein processing, cytoskeletal activities, and plant hormone responses. In another proteomic study done on the responses of A. thaliana seedlings to 3OC8-HSL treatment (Miao et  al. 2012), 53 proteins showed alteration in expression pattern, and 34 of these proteins were recognized to be associated with energy and carbohydrate metabolism, protein synthesis, plant defense, signal transduction, cytoskeleton remodeling, etc. The chloroplast was observed to be the most sensitive intracellular organelle to 3OC8-HSL treatment. Such findings strongly suggest that plant displayed extensive functional responses to bacterial AHLs that might be important for inter-kingdom interactions. In a recent proteomic study on the effect of exogenous AHLs on Arabidopsis thaliana seedlings under salinity stress, AHL application was found to impart salt tolerance and growth, and it might involve 97 proteins associated with defense/stress/detoxification, photosynthesis, protein metabolism, signal transduction, transcription, cell wall biogenesis, energy metabolisms, etc. (Ding et al. 2016).

2.3

AHL Impact on Plant Root Growth and Architecture

Mathesius and coworkers (2003) reported the activation of auxin-inducible GH3 promoter upon AHL application, from their proteomic analysis of M. truncatula roots post AHL treatment. In a later study, von Rad et al. (2008) also reported C6-­ HSL-­induced changes in the expression of several plant hormone-related genes, resulting in a higher expression of auxin and lower cytokinin concentrations. Moreover, they observed a significant increase in primary root growth in the presence of short-chain AHLs (C4-C6HSL) at 1 nM and a concentration above 10 micromolar (μΜ), respectively, in A. thaliana, whereas the long-chain C10-HSL remained

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neutral. The authors attributed this different plant response to the different acyl chain length of AHLs to the difference in their hydrophobicity. Long-chain AHLs with higher hydrophobicity are not transported from root to the shoot, and their accumulation in the root makes them toxic, thereby inhibiting the growth of root tissue. Since auxin induces root growth, the change in auxin/cytokinin ratio upon AHL treatment might be a potential mechanism behind short-chain AHL-induced root growth (von Rad et al. 2008). Modification of overall root architecture of A. thaliana on exposure to μΜ concentration of long-chain AHLs, especially C10-HSL, has been observed as a result of inhibition of primary root growth and promotion of lateral root and root hair growth (Ortíz-Castro et  al. 2008). This change in root morphology was associated with alterations in cell division and differentiation in the primary root meristem. Although auxin-treated Arabidopsis seedlings show similar changes in root morphology, C10-­ HSL action was independent of the auxin-regulated process. Enhanced lateral root and root hair growth could increase the absorptive capacity of the plant and also provide a larger surface area for bacterial colonization. These findings suggest the advantage of long-chain AHL-producing rhizobacteria to form a symbiotic association with the plant host. Short-chain C6-HSL has been shown (Schenk et al. 2012) to increase the shoot biomass and cause primary root elongation in Arabidopsis, with eventual decrease and loss of activity with an increase in acyl chain length (Fig. 2.1). Liu et al. (2012) demonstrated promotion of primary root growth in Arabidopsis by AHLs with modification at the C3 position of their branched chain, 3OC6-HSL and 3OC8-HSL treatment, in a concentration-dependent manner similar to C3 unsubstituted C6-HSL. On the other hand, long-chain AHLs, C12-HSL, and C14-HSL, promoted lateral root

Fig. 2.1  AHL influences plant root growth and morphology in Arabidopsis. Changes varied based on AHL acyl chain length. Short-chain AHLs (C6-HSL, C8-HSL) causes the growth of primary root, whereas long-chain AHL (C10-HSL) causes the growth of lateral root and root hair (von Rad et al. 2008; Bai et al. 2012; Liu et al. 2012)

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growth and inhibited root elongation, suggesting separate signaling pathways for the long- and short-chain AHLs (Liu et al. 2012). A different model plant, mung bean, was studied by Bai et al. (2012) for AHL treatment response. They found enhanced auxin-mediated adventitious root formation post AHL treatment. AHLs with C3 modification, particularly 3OC10-HSL, showed higher activity than their unmodified analogs such as C8-HSL, C10-HSL, and C12-HSL. This preference for specific AHL structures may be the result of spatial specificity, required by some plant proteins (Bai et al. 2012). In contrast to these reports, there was no significant effect on the growth of yam and barley plants when exposed to C6-HSL, C8-HSL, and C10-HSL (Götz-Rösch et al. 2015). These findings strongly suggest that different plants respond differently to AHLs, which may be a result of variations in AHL signaling cascades (Götz-Rösch et al. 2015). Figure created using BioRender.

2.4

AHL as Plant Strengthener

Plants possess a wide range of defenses that get activated in response to various stress, pathogens, and parasites (Gimenez et al. 2018). Induced resistance in plants is an important defense mechanism where defenses are preconditioned by prior infection or treatment resulting in resistance (or tolerance) against future infection (Vallad and Goodman 2004). The prior attack acts as a warning signal, preparing the plant for a stronger defense. The sensibilization mechanism, before an attack, called the priming phase, can be induced by a diverse range of low-molecular-weight metabolites and natural compounds, including AHLs (Mauch-Mani et al. 2017). Tomato plants get primed via SA- and ethylene-dependent defense genes, upon exposure to AHL-producing rhizobacteria, Serratia liquefaciens MG1, and Pseudomonas putida IsoF, against the fungal pathogen Alternaria alternata (Schuhegger et al. 2006). A similar AHL-mediated antifungal activity that involved on SA- and ethylene-related defense reactions was reported in cucumber (Cucumis sativus) by Serratia plymuthica HRO-C48 against the damping-off disease caused by Pythium aphanidermatum, as well as in bean and tomato plants against the gray mold fungus Botrytis cinerea infection (Pang et al. 2009). Among long-chain AHLs, 3-oxo-C14-HSL conferred systemic resistance in monocotyledonous (barley), and dicotyledonous plant (Arabidopsis) plants toward biotrophic and hemibiotrophic fungus, but not against necrotrophic fungal pathogens (Schikora et al. 2011). This resistance is associated with an increased expression of mitogen-activated protein kinases, AtMPK3, and AtMPK6, which consequently increases the expression of defense-related transcription factors, WRKY22 and WRKR29, and the Pathogenesis-Related1 gene (PR1). However, 3-oxo-C14-HSL did not show any impact on root and shoot growth as reported for long-chain AHLs (von Rad et  al. 2008). A similar effect of 3-oxo-C14-HSL imparting systemic resistance was reported by Zarkani et al. (2013) in A. thaliana when inoculated with Sinorhizobium meliloti strains producing oxo-C14-HSL. They observed that neither 3-oxo-C14-HSL-negative S. meliloti nor

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3-oxo-C8-HSL-positive Rhizobium etli produced a similar effect. These findings revealed that the resistance induced by AHLs does not necessarily require a hostsymbiont relationship to start with, as A. thaliana is not a symbiotic or noduleforming plant. Schenk et al. (2014) reported the priming effect of AHL on exposure to oxo-C14-­ HSL leading to increased deposition of lignin, phenolic compounds, and callose on the cell wall, reinforcing the cell wall to increase resistance to pathogens. A second possible mechanism of resistance by oxo-C14-HSL could be the enhanced stomatal closure observed due to AHL-induced accumulation of cis-12-oxo-phytodienoic acid (OPDA) and salicylic acid (SA) in plant leaves. Stomatal closure is an important part of innate immunity. Another interesting mechanism of resistance by AHL-­induced priming is the elevated level of hypersensitive response (HR) after infection. Barley primed with S. meliloti expR+ AHL showed accumulation of reactive oxygen species (ROS) and increased expression of Peroxidase7 as an HR, following infection with Blumeria graminis (Hernández Reyes et al. 2014). Given these various mechanisms of resistance induced by AHL priming, AHL-induced resistance seems to differ from the systemic acquired and the induced systemic resistances, providing new insight into inter-kingdom communication (Schenk et  al. 2014). Moshynets et  al. (2019) used C6-HSL as a seed primer for winter wheat (Triticum aestivum L.), which was found to improve germination levels significantly, biomass at filtering stage, crop structure, and productivity at maturity of the crop. Thus, AHLs could find application in improving growth and productivity of cereal crops.

2.5

Effect of AHL on Symbiosis and Nitrogen Cycle

Many strains of nodulating rhizobia such as Rhizobium leguminosarum bv. viciae, R. leguminosarum, S. meliloti Rm41, and A. tumefaciens are associated with quorum sensing gene regulation systems (Gonzalez and Marketon 2003). The process of legume-host symbiosis is a complex interplay of communication between various signal molecules that includes flavonoids from root exudates that attract the rhizobia, exopolysaccharides for bacterial attachment, Nod factors for initiation of root cell division to form the infection threads, and AHLs. Once bacteria reach the host, a further process of symbiosis depends on reaching a threshold cell density, coordinated by the QS regulatory system (Gonzalez and Marketon 2003; Sanchez-­ Contreras et al. 2007; Downie 2010). A few QS regulatory systems directly linked to symbiosis are discussed here. Association of root nodule formation with an unidentified AHL was initially reported in Rhizobium leguminosarum by Gray et  al. (1996). Rosemeyer et  al. (1998) identified luxI- and luxR-homologous genes, raiI, and raiR in Rhizobium etli CNPAF512 and found raiI to have a restrictive effect on the number of nodules in the host plant Phaseolus vulgaris without affecting the nitrogen-fixing capacity per nodule. On the other hand, the second quorum sensing locus, cinI, and cinR in Rhizobium etli CNPAF512 was essential for nodule bacteroid differentiation and involved in symbiotic nitrogen fixation (Daniels et  al. 2002). However, the same

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genes showed varying implications in different Rhizobium strains. Mutation of cinR and cinI in R. leguminosarum had little or no effect on the growth of the bacterium and in the symbiosis with peas (Edwards et al. 2009). QS-deficient mutants of Mesorhizobium huakuii showed an inability to form root nodules (Gao et al. 2006). MrtI-MrtR pair was identified as LuxI-LuxR homologs in M. tianshanense and played an indispensable role in root hair adherence and nodulation on the host plant Glycyrrhiza uralensis; QS-deficient mutants showed the absence of nodulation (Zheng et al. 2006; Cao et al. 2009). Increase in several nodules was observed in M. truncatula after treatment with 1 μM 3-oxo-C14-HSL with no effect on lateral root number (Veliz-Vallejos et al. 2014). Study on ExpR/Sin QS system in Sinorhizobium meliloti by Gurich and González (2009) revealed that QS stays active during all the growth phases till symbiosis is established, after which the bacteroids’ metabolic functions focus on nitrogen fixation. Besides nitrogen fixation, nitrogen mineralization is also responsible for providing plants the utilizable form of nitrogen, where microbes enzymatically break down the organic nitrogen sources such as chitin, to the simpler inorganic form of nitrogen such as ammonia. DeAngelis et al. (2008) studied the link between QS and extracellular enzyme activity of 533 bacterial isolates, dominated byα-proteobacterial isolates such as Agrobacterium rhizogenes, Inquilinus ginsengisoli, and Burkholderia sp. in the rhizosphere of Avena and observed compromised chitinase or protease activity in all but one isolates upon disruption of QS. This strongly suggests that QS plays an important role in the regulation of exoenzyme production by bacteria in soil, and thus targeting QS for disease control should also take into account the resultant risk of disturbing soil nitrogen cycle.

2.6

AHL-Induced Plant Diseases

Phytopathogenic bacteria employ QS regulatory system to control virulence and may carry one or more QS regulons. The most well-characterized bacterial signal molecules involved in plant pathogenesis include AHLs, DSF, and 3-hydroxy palmitic acid methyl ester or methyl 3-hydroxypalmitate (Sibanda et al. 2016). The LuxR homologs aviR, avsR, and avsI in Agrobacterium vitis are required for causing necrosis in grapes and hypersensitive-like response on tobacco (Zheng et al. 2003; Hao et al. 2005; Hao and Burr 2006). Ferluga et al. (2007) reported a LuxR family-type regulator, OryR, in Xanthomonas oryzae pv. oryzae (Xoo), essential for virulence in rice, and it required macerated rice for activity. The plant pathogen, Pantoea ananatis SK-1 depends on the quorum sensing system for the biosynthesis of extracellular polymeric substances (EPS), biofilm formation and causes center rot disease in onion (Morohoshi et al. 2007). Liu et al. (2008) demonstrated a greater role for QS in pathogenesis as a “master regulator,” controlling other regulatory systems that further coordinate to control virulence genes. The study monitored the progression of soft rot in potato caused by P. atrosepticum using virulence factors and plant cell wall-degrading enzymes (PCWDEs) under the control of the QS system. Differential transcription of up to

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26% of the P. atrosepticum genome was observed in a QS mutant. They also identified many novel components of the QS regulon namely type I, II secretion systems associated with secretion of PCWDE; type III secretion system and coronafacoyl-­ amide conjugates for manipulation of plant defenses; T6SS (Type VI secretion system) and VirS, a novel potential regulator essential for complete virulence. It is interesting how some plant pathogens exploit changes in plant chemicals to mount an optimal attack. This is a common phenomenon among plant pathogens carrying the “orphan or the solo” LuxR homologs, which do not possess a cognate LuxI homolog (Subramoni and Venturi 2009). LuxR solos occur in both AHL-­ producing and AHL-nonproducing bacteria, allowing them to respond to signals from other bacteria or eukaryotes. These LuxR solos may act as important interspecies and inter-kingdom signals (Ferluga and Venturi 2009; Subramoni and Venturi 2009). For example, OryR protein of Xanthomonas oryzae pv. oryzae, solubilized in the presence of rice extract, however became insoluble in the presence  different AHLs. This indicates the presence of a molecule in rice extract that might interact with and stabilize OryR (Ferluga et al. 2007) and that this molecule could be closely related to AHLs, as OryR possesses an AHL-binding motif. Similarly, XccR, the LuxI homolog in Xanthomonas campestris pv. campestris, causes infection in cabbage. XccR associates with an unknown plant factor and binds to a lux-box present in the promoter of the proline aminopeptidase (pip) virulence gene (Zhang et  al. 2012). It is probable that OryR, XccR solos, and their plant partner participate in inter-kingdom signaling, and identification of the plant compounds would set novel insights into inter-kingdom signaling (Subramoni and Venturi 2009).

2.7

 HL Uptake in Plant and Possible Signaling Pathways A for Plant Response to AHL

There are a few reports addressing this basic question of whether AHLs coordinate with other signals upon perception by plant or are taken up by plants by some physical mechanism (Schikora et al. 2016). Götz and coworkers (2007) tested the uptake of radiolabeled C6-HSL, C8-HSL, and C10-HSL in barley (Hordeum vulgare L.) and yam (Pachyrhizus erosus L.). Ultra-performance liquid chromatography (UPLC) and Fourier transform ion cyclotron resonance mass spectrometry (FTICR-MS) analysis revealed short AHLs, only C6-HSL, and C8-HSL, transported from roots into barley shoots and C6-HSL in case of yam shoots. A. thaliana also transported C6-HSL from root to leaves in a time-dependent manner, while C10-HSL remained accumulated in root region (von Rad et al. 2008). Similarly, it was observed that the long-chain AHLs, oxo-C14-HSL, were not taken up within the Arabidopsis plant. Moreover, it showed no effect on root growth, whereas short-chain AHL C6-HSL got systemically translocated from root to shoot and affected growth-promoting effect (Schikora et al. 2011). A possible reason behind the difference in uptake of AHLs might be the reduced motility with an increase in acyl chain length or higher hydrophobicity of longer AHLs (von Rad et al. 2008; Schikora et al. 2011).

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However, Sieper et al. (2014) reported systemic transport of C8-HSL and C10-HSL into the barley shoots with a molecular analysis of the process backed by autoradiography analysis, sensor strain assays, and monoclonal antibodies. They suggested a probable active or semi-active process of translocation of AHLs with the involvement of ATP-binding cassette (ABC) transporters based on the inhibition of AHL uptake in the presence of orthovanadate, an inhibitor of ABC transporters. All these reports point toward different signaling pathways and receptors for different AHLs. Götz-­Rösch et  al. (2015) observed a distinct pattern of selected detoxification enzymes activity in barley and yam plants, upon C6-, C8-, and C10-HSL treatment. The activities of glutathione S-transferase and ROS scavenging enzymes were mostly tissue specific. C6-HSL was readily transported into all barley plant parts without degradation with the most prominent influence on the leaf-located enzymes. On the other hand, the yam plant showed no such change in detoxification enzyme activity, which might be a result of the absence of AHL-transport machinery toward the shoot in yam bean. In both the plants, C10-HSL was almost broken down completely before it entered the shoot in its initial form. Interestingly, the metabolization was faster in yam plant than in barley, which may be related to the fact that symbiotic yam beans are naturally exposed to AHL (Götz-Rösch et al. 2015). Other studies have aimed at deciphering the molecular mechanisms behind the plant-AHL interactions, such as AHL perception mechanism in plant and signal transduction pathways involved (Jin et al. 2012; Song et al. 2011; Liu et al. 2012; Zhao et al. 2016). G-protein signaling is considered one of the most conserved signaling pathways in plants and is associated with the transduction of many extracellular signals. It is involved in many physiological functions in plants like stomatal opening (Urano and Jones 2013), phytochrome-dependent cell death (Zhang et al. 2012), stress signaling (Tuteja and Sopory 2008), response to plant hormones, and agronomical traits like nitrogen fixation, seed size, and number (Pandey et al. 2019). In typical G-protein signaling, the G-protein complex comprised of Gα, Gβ, and Gγ subunits remains inactive with GDP bound to the Gα subunit. In animals, the G-proteins get activated via a membrane protein called G-protein-coupled receptor (GPCR) upon binding with a ligand, leading to the exchange of GTP with GDP and the dissociation of GTP-Gα from the Gβγ subunit. The free Gα and Gβγ subunits further initiate different intracellular signaling pathways (Tuteja 2009). However, in plants, the G-protein signaling is reported to be independent of GPCR, and the plant G-proteins release GDP spontaneously and thus are self-activating (Urano and Jones 2013). Although some authors  think this hypothesis is supported by genetic and physiological findings, it is still not clear whether the hypothesis applies to all G-proteins in all plant species (Pandey et  al. 2019). Song et  al. (2011) hypothesized that AHLs in plants is received by GPCRs, which activate the G-protein α subunit and Ca2+ channels to allow Ca2+ influx. C4-HSL treatment on A. thaliana roots was shown to cause a transient rise in cytosolic Ca2+ as a result of influx from the extracellular matrix. The authors suggest Ca2+ signaling might help plant cells to sense QS signals. However, considering the possibility of the absence of GPCR, AHL might also interact directly with intracellular receptors without the help of transmembrane proteins (Jin et al. 2012; Song et al. 2011). Many G-protein-coupled receptors (GPCRs) have been reported to mediate AHL-induced root elongation in A. thaliana. Expression of GPCRs, Cand2, Cand7

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(Jin et al. 2012), GCR1, and GCR2 (Bian et al. 2011) increased in A. thaliana root in response to 1 μΜ 3OC6-HSL and 10 μΜ 3OC8-HSL treatment. GPA1 was also added to this list of GPCRs affecting 3OC6-HSL and 3OC8-HSL action on root growth in A. thaliana in a concentration-dependent manner (Liu et  al. 2012). Involvement of H2O2 and NO-dependent cGMP signaling pathways behind this AHL-induced auxin-dependent lateral root formation has also been proposed (Bai et al. 2012). A recent report on 3OC6-HSL enhancing root elongation involves the transcriptional factor AtMYB44 in A. thaliana (Zhao et al. 2016).

2.8

Plant Interference with QS Signals

Not only do plants respond to AHL and QS systems in various ways, from reaping symbiotic benefits to enhancing disease resistance, they also evolve strategies to interfere with the microbial signaling systems for their advantage, by producing signal mimics, certain plant metabolites, and signal-degrading enzymes (Fig. 2.2).

2.8.1 Plant Interferes with QS via AHL Mimics AHL mimic compounds are reported to be produced by many plants to create confusion in microbial communication (Bauer and Mathesius 2004). Halogenated furanones from Delisea pulchra, a marine red alga, were reported to have strong

Fig. 2.2  Schematic presentation of how plants resist and manipulate QS signaling to their advantage. Figure created using BioRender

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inhibitory effects against AHL-controlled phenotypes in Serratia liquefaciens, Escherichia coli, and Proteus mirabilis models (Givskov et al. 1996; Gram et al. 1996). Later, the structural similarity of furanones to AHLs was confirmed alongside their possible mode of action of displacing AHLs competitively from the AHL LuxR receptor (Manefield et al. 1999). Further clarity into the mechanism of furanones came from the finding that halogenated furanones destabilized LuxR protein, accelerating its degradation (Manefield et al. 2002). The leaves and stem of rice plants produce AHL mimics, which could activate three different bacterial AHL biosensors and were very sensitive to the AiiA lactonase. Given the highly specific nature of lactonases, these rice compounds may be another AHL or a compound of close structure (Degrassi et al. 2007). Teplitski et al. (2000) reported the presence of AHL mimics in pea seedling exudates using various AHL reporter strains, C. violaceum CV026, P. aureofaciens 30-84I, and S. liquefaciens MG44. Activity analysis of different HPLC fractions revealed the presence of both inhibitory and stimulatory substances in pea plant. AHL mimic activity was also shown by seedlings of other plant species, rice, soybean, tomato, crown vetch, and Medicago truncatula, suggesting AHL mimic synthesis is a common response among higher plants (Helman and Chernin 2015). Gao et al. (2003) reported around 15 to 20 separable unidentified QS mimic compounds in M. truncatula young seedling, capable of specifically stimulating or inhibiting responses in QS reporter bacteria, Vibrio harveyi BB170, Pseudomonas putida pAS-C8, C. violaceum CV026, and E. coli strains JM109, p(SB401), p(SB536), and p(SB1075). However, the precise chemical structure of these QS mimics in pea, rice, and M. truncatula is not yet known, except for the possibility of a structure close to that of AHLs. It is also suggested that such mimic compounds might be degradation products of bacterial AHLs as the result of the action of plant AHL-degrading enzymes such as lactonases (Mathesius and Watt 2010). Pérez-Montaño et  al. (2013) reported AHL mimic molecules produced by Oryza sativa (rice) and P. vulgaris (bean) plants that specifically interfere with the QS-regulated biofilm formation of two plant-­ associated bacteria, Sinorhizobium fredii SMH12 and Pantoea ananatis AMG501. These mimic compounds are considered non-AHL-type mimics as they lack a lactone ring typical of AHLs. Seed and root exudates of Arachis hypogaea L. (peanut) contain unidentified long-chain AHL-like mimics and short inhibitory chain AHLlike compounds, which are tools for manipulating the bacterial behavior in the rhizosphere (Nievas et al. 2017).

2.8.2 Plant Metabolites and Enzymatic Interference of QS Many plant secondary metabolites interfere directly and indirectly with bacterial QS. Keshavan et al. (2005) coined the term quorum sensing-interfering (QSI) compounds for the second group of plant signals that do not resemble AHLs. They observed inhibition of violacein production in C. violaceum CV026 by Alfalfa seed and seedling exudates without affecting cell growth, indicating interference of QS. Structural characterization of a molecule purified from the exudates revealed it

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as L-canavanine, an arginine analog. The Alfalfa seed exudates also inhibited the synthesis of exopolysaccharide EPS II, QS-regulated phenotype, required for establishing symbiosis in S. meliloti, the natural symbiont of Alfalfa. A similar effect was demonstrated by synthetic L-canavanine, which did not affect protein synthesis or synthesis of AHL in S. meliloti. A possible mechanism of action may be the incorporation of L-canavanine in place of L-arginine in the QS regulator protein, thus impairing protein folding. Alternatively, some bacteria such as Streptococcus faecalis can degrade L-canavanine to homoserine (Kalyankar et al. 1958), which if converted to AHL mimic scan also contribute to the QS inhibition property of L-canavanine. Salicylic acid (SA) produced by plants downregulates the virulence genes and activates the quorum degradation system, attKLM operon in Agrobacterium, which includes the attM gene encoding a lactonase (Yuan et al. 2007). Thus, SA might act as a powerful plant defense signal acting against Agrobacterium and other QS bacteria in the phytobiome. A similar interference with QS mechanism was observed when plant phenolic acids, cinnamic acid (CA), and SA inhibited expression of QS regulator gene; QS regulated virulence genes and reduced AHL level in Pectobacterium aroidearum and P. carotovorum (Joshi et al. 2016). Cinnamaldehyde is a naturally occurring compound in the bark of cinnamon trees and widely used in food industries. Niu et al. (2006) reported inhibition of 3-hydroxy-C4-HSL- and 3OC6-HSLmediated QS by very low concentrations of synthetic cinnamaldehyde. p-Coumaric acid, a natural phenolic compound produced by plants, showed both stimulatory and inhibitory effects on QS in a concentration- and strain-dependent manner, whereas garlic extract inhibited QS receptors LuxR, AhyR, and TraR, which become toxic at higher concentrations (Bodini et al. 2009). It is interesting that coumaric and cinnamic acids have also been implicated in the synthesis of aryl HSL signals in certain nodulating rhizobacteria (Schaefer et al. 2008; Ahlgren et al. 2011). The vitamin riboflavin and its derivative, lumichrome, are synthesized by bacteria such as B. subtilis, E. coli, Photobacterium phosphoreum, and Actinobacillus pleuropneumoniae (Vitreschak et al. 2002), a majority of plants (Roje 2007), and algae like Chlamydomonas (Palacios et al. 2014). Riboflavin and lumichrome purified from the green alga Chlamydomonas reinhardtii can bind to and activate the AHL receptor LasR and thus interfere with bacterial QS (Rajamani et  al. 2008). Change in response to riboflavin and lumichrome after mutation of LasR residues required for AHL binding indicated a similar binding site for all the three signals. These molecules may have a larger and complex role, given the fact that they are produced by plants, bacteria, and algae (Mathesius and Watt 2010). Medicinal plants also contribute a vast repertoire of secondary metabolites with anti-QS effects. Curcumin, the phenolic bioactive compound of Curcuma longa (turmeric), is a popular example. It can attenuate Pseudomonas aeruginosa (PAO1) virulence by interfering with AHL production, biofilm formation, and inhibiting elastase and protease activity (Rudrappa and Bais 2008). It is associated with reduction in biofilm formation by uropathogens, E. coli, Proteus mirabilis, P. aeruginosa, and Serratia marcescens that cause persistent urinary tract infection via QS-dependent virulence mechanisms (Packiavathy et  al. 2014). Some eminent

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examples of medicinal plants with anti QS activity include Terminalia chebula, Ocimum sanctum, Amphipterygium adstringens, and Centella asiatica (Bouyahya et al. 2017). The primary bioactive compounds present in these medicinal plants are polyphenols, terpenoids, flavonoids, quinines, tannins, anthocyanins, polyamines, cytokinins, and polysaccharides (Bouyahya et al. 2017). Many plant volatiles such as essential oils (EO) and their components compounds also act as a signal and affect bacterial QS (Ahmad et al. 2015). Eucalyptus globulus and E. radiate essential oils contain eucalyptol and limonene as the main bioactive component, respectively, which inhibited violacein pigment of the reporter strain C. violaceum CV026 without changing cell growth parameters, indicating antiquorum sensing activity (Luís et al. 2016). A similar effect was seen in EOs from different species of Piper (Olivero et al. 2011). Khan et al. (2009) reported the anti-QS property of an unknown component of clove oil, whereas eugenol, the main constituent of clove oil, could not inhibit QS activity, indicating the anti-QS property of other minor components of the oil such as α-caryophyllene and β-caryophyllene. Citrus reticulate EOs also showed inhibition of biofilm formation and AHL production (Luciardi et al. 2016). Thymus vulgare EO inhibited the expression of the AHL-related flagella gene flgA required for initial bacterial attachment for biofilm formation by the foodborne pathogen P. fluorescens KM121 strain (Myszka et al. 2016). The significance of the AHL-based signaling systems is reflected in the abundance of quorum quenching activities in plants and animals, which have the role of destroying the signaling activity of bacterial pathogens (Schikora et al. 2016). Plants can interfere with bacterial QS by producing enzymes as well. Delalande et  al. (2005) reported rapid disappearance of AHLs from the root region of germinating Lotus plants, and a possible enzymatic mechanism is suspected. AHLs are reported to alter Arabidopsis postembryonic root development  (Ortíz-Castro et  al. 2008). Fatty acid amide hydrolase expressed by Arabidopsis could degrade AHLs, as evident from the increased resistance to AHLs in overexpressing mutants, and AHLs induced susceptibility to developmental changes in fatty acid amide hydrolase mutant (Ortíz-Castro et al. 2008).

2.9

Role of Endophyte in a Phytobiome

Endophytes are microbes that symbiotically live whole or at least a part of their life cycle within a living plant without showing any signs of infection. However, commonly known endophytes are mostly considered commensals and do not affect host plant functioning, while less common are either mutualistic with beneficial effects or antagonistic as latent pathogens (Hardoim et al. 2015). The beneficial effects of an endophyte include the promotion of plant growth, health, and contribution to host defense response against a pathogen and abiotic stresses (Khare et al. 2018). One of the most notable properties of endophytes is their ability to either synthesize or induce a host plant to synthesize metabolites that promote plant growth and help them adapt better to the environment (Varma et al. 2017). Thus, they promise eco-­ friendly sources of useful bioactive compounds such as antibiotics and anticancer

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drugs (Hardoim et  al. 2015). Moreover, endophytic make up of edible plants becomes a concern as it is known that some plant-friendly endophytes could be potential human pathogens (van Overbeek et al. 2014). Although it is accepted that the interaction of endophyte and its host plant may be multidimensional (Khare et al. 2018), many fundamental questions remain to be answered. How do plants recruit endophytes (Kandel et al. 2017)? How does the endophyte survive the first line of defense of the host plant? How do they influence host gene expression and how different members of the endophyte community interact and influence one another? There are a few reports on QS activity among endophytes and about its influence on the host plant. Hudson et  al. (2010) isolated and identified several culturable endophytic strains from stem tissue of sugarcane and from xylem fluids of grapevine. Five of six sugarcanes and fourteen of fifteen grapes with identified endophytes showed a significant response in at least one AHL-dependent biosensor. AHL lactonase activity has been reported in endophytic population isolated from potato tuber peel (Ha et al. 2018) and Pterocarpus santalinus (Rajesh and Rai 2014). Two AHL-based quorum sensing systems, SplIR and SpsIR, have been reported from endophytic Serratia sp. strain G3 (Liu et al. 2011). While similar to the free-living strain of Serratia HROC48,  antifungal activity, indole-3-acetic acid and exoenzyme production in the G3 strain are regulated by QS,  however, QS control of swimming motility and biofilm formation was a strain-specific phenotype, reflecting a lifestyle driven by the evolution of the QS systems in free-living and endophytic strains. Jiang et al. (2014) reported production of 3OC8-HSL by Pantoea agglomerans YS19, an endophytic diazotrophic bacterium isolated from rice, and revealed the importance of 3OC8-HSL in promoting bacterial growth and also in the formation of a multicellular aggregate structure called symplasmata, which is a characteristic of the bacterium. Pseudomonas sp. strain GM79, an endophyte isolated from cottonwood (Populus deltoides), possesses an orphan OryR homolog PipR, which was shown to require an unknown signal derived from the cottonwood leaf macerates instead of an AHL (Schaefer et al. 2016). The signal was later identified as a chemical derived from ethanolamine activity (Coutinho et al. 2018). Similar roles of plant signals for activation of different solo/orphan Lux R homologs have been reported in many other free-living bacteria (Ferluga et al. 2007; Ferluga and Venturi 2009; Subramoni and Venturi 2009). Thus, the current understanding of endophytes signifies their immense potential and advantage in improving the quality of a phytobiome. At the same time, the need for a deeper understanding of the physiology of endophytes is also obvious, given the limited number of reports and a nonsystemic approach of study used so far (Hardoim et al. 2015).

2.10 Conclusion and Forthcoming Prospects Managing the phytobiome may offer an important biotechnological area for improving agricultural yield and quality with a minimum participation of harmful agrochemicals. Phytobiome studies may provide more precise insights into the

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mechanisms and consequences of disease (and resistance) and identify microbial indicators of disease (and resistance) progress. In the field, it can be assumed that communication signals are exposed to many interfering and mimic signals from the neighbors, and hence a system-level understanding of phytobiome is the appropriate approach for successful application of this understanding. One of the pivotal points of control to bring desired traits in a phytobiome is the manipulation of the interspecies and intraspecies communication between plants and microbes, either by introducing selected beneficial microbes as microbial biofertilizers and biopesticides or by genetic engineering of plants and microbes. A known plasmid pME6863 carrying a lactonase coding gene aiiA from Bacillus sp. A24 to Pseudomonas fluorescens P3 exhibited the ability to degrade AHLs and significantly reduced soft potato rot caused by Erwinia carotovora and crown gall of tomato caused by Agrobacterium tumefaciens to a similar level as Bacillus sp. A24. Tobacco and potato plants transformed with AHL lactonase from Bacillus sp. showed enhanced resistance to E. carotovora infection. The use of advanced “omic” technologies, such as metabolomics and proteomics, allows a more reliable analysis of phytobiome interactions in unprecedented detail and provides insights into the resistance mechanisms that consider both simultaneous attacks of various pathogens and the interplay with beneficial microbes. In this context, the metagenomic study of unculturable microorganisms would also provide an indispensable solution to this whole complex equation in a phytobiome. Moreover, a multidisciplinary analysis should be incorporated by collaborative discussions among different disciplines such as biologists, ecologists, plant pathologists and agricultural entomologists. It should be soon possible to provide a systemic picture of how and to what extent plants can shape their own detrimental or beneficial community.

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Schikora A, Schenk ST, Stein E, Molitor A, Zuccaro A, Kogel KH (2011) N-acyl-homoserine lactone confers resistance towards biotrophic and hemibiotrophic pathogens via altered activation of AtMPK6. Plant Physiol 157:1407–1418 Schikora A, Schenk ST, Hartmann A (2016) Beneficial effects of bacteria-plant communication based on quorum sensing molecules of the N -acyl homoserine lactone group. Plant Mol Biol 90(6):605–612 Schuhegger R, Ihring A, Gantner S, Bahnweg G, Knappe C, Vogg G, Hutzler P, Schmid M, Van Breusegem F, Eberl LE, Hartmann A (2006) Induction of systemic resistance in tomato by N-acyl-L-homoserine lactone-producing rhizosphere bacteria. Plant Cell Environ 29(5):909–918 Sibanda S, Theron J, Shyntum DY, Moleleki LN, Coutinho TA (2016) Characterization of two LuxI/R homologs in Pantoea ananatis LMG 2665T. Can J Microbiol 62(11):893–903 Sieper T, Forczek S, Matucha M, Krämer P, Hartmann A, Schröder P (2014) N-acyl-homoserine lactone uptake and systemic transport in barley rest upon active parts of the plant. New Phytol 201(2):545–555 Song S, Jia Z, Xu J, Zhang Z, Bian Z (2011) N-butyryl-homoserine lactone, a bacterial quorum-­ sensing signaling molecule, induces intracellular calcium elevation in Arabidopsis root cells. Biochem Biophys Res Commun 414(2):355–360 Subramoni S, Venturi V (2009) LuxR-family ‘solos’: bachelor sensors/regulators of signalling molecules. Microbiology 155(5):1377–1385 Teplitski M, Robinson JB, Bauer WD (2000) Plants secrete substances that mimic bacterial N-acyl homoserine lactone signal activities and affect population density-dependent behaviors in associated bacteria. Mol Plant-Microbe Interact 13(6):637–648 Tuteja N (2009) Signaling through G protein coupled receptors. Plant Signal Behav 4(10):942–947 Tuteja N, Sopory S (2008) Plant signaling in stress: G-protein coupled receptors, heterotrimeric G-proteins and signal coupling via phospholipases. Plant Signal Behav 3:79–86 Urano D, Jones AM (2013) “Round up the usual suspects”: a comment on nonexistent plant G protein-coupled receptors. Plant Physiol 161(3):1097–1102 Uroz S, Dessaux Y, Oger P (2009) Quorum sensing and quorum quenching: the yin and yang of bacterial communication. Chembiochem 10(2):205–216 Vallad EG, Goodman MR (2004) Systemic acquired resistance and induced systemic resistance in conventional agriculture. Crop Sci 44:1920–1934 van Overbeek LS, van Doorn J, Wichers JH, van Amerongen A, van Roermund HJW, Willemsen PTJ (2014) The arable ecosystem as battleground for emergence of new human pathogens. Front Microbiol 5:1–17 Varma PK, Uppala S, Pavuluri K, Chandra KJ, Chapala MM, Kumar KV (2017) Endophytes: role and functions in crop health. In: Plant-microbe interactions in agro-ecological perspectives. Springer, Singapore, pp 291–310 Veliz-Vallejos DF, van Noorden GE, Yuan M, Mathesius U (2014) A Sinorhizobium meliloti-­ specific N-acyl homoserine lactone quorum-sensing signal increases nodule numbers in Medicago truncatula independent of autoregulation. Front Plant Sci 5:551 Venturi V, Keel C (2016) Signaling in the rhizosphere. Trends Plant Sci 21:187–198 Vitreschak AG, Rodionov DA, Mironov AA, Gelfand MS (2002) Regulation of riboflavin biosynthesis and transport genes in bacteria by transcriptional and translational attenuation. Nucleic Acids Res 30(14):3141–3151 von Rad U, Klein I, Dobrev PI, Kottova J, Zazimalova E, Fekete A, Hartmann A, Schmitt-Kopplin P, Durner J (2008) Response of Arabidopsis thaliana to N-hexanoyl-DL-homoserine-lactone, a bacterial quorum sensing molecule produced in the rhizosphere. Planta 229(1):73–85 Williams P (2007) Quorum sensing, communication and cross-kingdom signaling in the bacterial world. Microbiology 153(12):3923–3938 Witzany G (2006) Plant communication from biosemiotic perspective: differences in abiotic and biotic signal perception determine the content arrangement of response behavior. Context determines the meaning of meta-, inter-and intraorganismic plant signaling. Plant Signal Behav 1(4):169–178

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3

Plant Microbiomes: Understanding the Aboveground Benefits Mohini Prabha Singh, Pratiksha Singh, Rajesh Kumar Singh, Manoj Kumar Solanki, and Sumandeep Kaur Bazzer

Abstract

Soil and plant root are known as the microbial reservoir, and these microbes are found broadly in the plant rhizosphere and tissues. Phytobiome generally exists as epiphytic, endophytic, and rhizospheric that undertakes a critical role in plant development. These microbiomes may shape networks, to stabilize the function among different kinds of plant-associated factors to propagate or transmit in a different part of the plant. Microbial networks linked with plant health give crucial beneficial insights to look upon. The present section covers the features of such microbial networks that build the phytobiome. The chapter highlights their ability to better uptake nutrients or plant growth regulators in a stressed environment and further extends an evolution of studies depicting the supporting components that shape the phylogenetic and plant-related networks. The chapter advocates the possibility to understand the techniques by which plants select and connect with their microbiomes and affect plant improvement and well-being, thereby laying the foundation of novel microbiome-driven systems to the advancement of sustainable agriculture. The microbiome is unpredictably

M. P. Singh (*) Punjab Agricultural University, Ludhiana Punjab, India P. Singh · R. K. Singh Guangxi Key Laboratory of Sugarcane Biotechnology and Genetic Improvement (Guangxi), Ministry of Agriculture, Sugarcane Research Institute, Chinese Academy of Agricultural Sciences, Guangxi Academy of Agricultural Sciences, Nanning China M. K. Solanki Department of Food Quality & Safety, Institute for Post-harvest and Food Sciences, The Volcani Center, Agricultural Research Organization, Rishon LeZion Israel S. K. Bazzer Department of Crops, Soil, and Environmental Sciences, University of Arkansas, Fayetteville AR, USA © Springer Nature Singapore Pte Ltd. 2020 M. K. Solanki et al. (eds.), Phytobiomes: Current Insights and Future Vistas, https://doi.org/10.1007/978-981-15-3151-4_3

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engaged with plant well-being providing extra qualities to the plant. To ­understand the guideline of plant characteristic articulation, henceforth plant execution, and how this impacts the biological systemic network, it is required to get well versed with phytobiome and its usefulness. In the present section, the significance of the phytobiome to plant genomics is tended to describe the phytobiome in assembly to the environment of the outline with attention on natural surroundings happening subterranean at the plant-soil between face, where the center is around the job of exudates as currency in this framework. Keywords

Microbial communities · Rhizosphere · Endophytes · Phyllosphere

3.1

Introduction

Nature allows the coexistence of healthy and asymptomatic plants with diverse microbes such as archaea, bacteria, fungi, and protists where a complex microbial consortium is formed to impact plant growth and productivity (Vorholt 2012; Kumari et al. 2019; Solanki et al. 2019). Phytobiome has either neutral or helpful roles in the plants’ fitness (Mendes et  al. 2013). The useful impacts on plants include disease suppression (Ritpitakphong et al. 2016; Solanki et al. 2012), plant immunization (Van der Ent et al. 2009), induction of systemic resistance (Zamioudis et al. 2015), increased nutrient acquisition (Van der Heijden et al. 2016), increased tolerance to abiotic stresses (Rolli et  al. 2015; Wang et  al. 2018), adaptation to environmental variations (Haney et al. 2015), or enhancement of the mycorrhizal colonization (Garbaye 1994). Microorganisms can also target agricultural productivity by providing nutrient availability/acquisition (Kavamura et al. 2013). Lack of precise methodologies has led to limited access to nonculturable microbial groups, and thus, most of the work relies on single microbial groups associated with plants (Andreote et al. 2009). Mycorrhizal association with a plant (Chagnon et al. 2013) and microbial diazotrophs (Raymond et al. 2004) are the few examples that need to be explored in-depth. Nevertheless, an inclusive map of this system laid stress on the interactions happening between diverse groups of microbes, permitting the term “microbiome.” Joshua Lederberg coined the term “microbiome” for the first time and described it to be the “ecological community of commensal microorganisms, symbionts or pathogens that occupy a space in our body” (Lederberg and McCray 2001). New terminology for “microbiome” was suggested by Boon et al. (2014) that relates to host-associated genes in a defined surrounding, thereby bypassing the abundance of the microbial community of low significance. Plant-associated microbial groups work in multidimensional ways as host plant delivers unique metabolic adeptness to attract beneficial microbial niches that can have a positive (mutualistic), neutral (communalistic), or deleterious (pathogenic)

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effect on plant health (Thrall et  al. 2007). Microbes are the main component of plant functional traits such as soil formation, organic matter decomposition, nutrient mobilization, and improvement in plant productivity (deBello et  al. 2010). Rhizospheric prokaryotes are known as plant helpers due to their beneficial activities such as nitrogen (N2) fixation (Martinez-Romero 2006), solubilization of insoluble minerals, and stimulation of phytohormones (Hardoim et  al. 2008). Genome duplication (polyploidization) is defined as macroevolutionary events of host that can change microbiome structure. The phytobiome exerts influences on plant trait expression through upstream and downstream regulation of nutritional uptake, thus supervising plant’s performance. To unlock the subtleties inside the ecosystem, and the regulation of plant trait expression, impacts of the microbiome are needed to be observed. Bernedsen et al. (2012) reported that plant microbiome interface aligned as “microbe-soil-microbe-plant-microbe interface” rather than the “soil-microbe-plant interface.” Plant genome is itself a complex system, and microbial interaction is coined as the plant’s “second genome” because it extends the plants’ genetic compendium extensively. This chapter also contains a detailed description of beneficial phytobiome interactions. Three microbial groups (bacteria, fungi, and protists) that abundantly originate on plant tissues are deliberated, and diverse mechanisms used to cooperate and compete in planta are defined. Nevertheless, the activity of microbiomes is a new systematic approach that is required to understand the multidimensional actions of microbial communities (Bashiardes et  al. 2018). To some degree, microbiome applications would include an emphasis on enlightening basic components that can improve crop production such as management of plant nutrients, soil health, and environmental safety (Syed Ab Rahman et al. 2018).

3.2

Soil Microbiome Characterization

Phytobiomes are discrete that comprise unfavorable pathogens, potential endophytes, and helpful symbionts (Rosenblueth and Martínez-Romero 2006; Wang et  al. 2017; Malviya et  al. 2019). Be that as it may, traditionally, the microbial assorted variety was assessed by segregating and refined on various supplement media and development conditions. Microbial metabolism fulfills the nutritional and regulatory prerequisites of plants (Lugtenberg and Kamilova 2009). These healthful necessities, for the most part, incorporate nitrogen, phosphorous, and iron. Moreover, these elements also control plant growth by stimulating the production of plant growth regulators. Screening of the most suitable bacteria would require culture-­based methods (Taulé et al. 2012). On a routine basis, the procedures normally contain an agar plate assay or a broth medium to multiply the microbes. These assays also help in locating genetic components of microbes. However, these protocols failed to explore the microbial diversity of nonculturable microbiota. For investigating the entire microbiome, the very first effort is initiated with sequencing of a conserved gene region such as the 16S rRNA gene that is widely

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applied for microbial identification (Mullis et al. 1987). To contemplate and comprehend the microbiome in a brief span, thorough upgrades have been accomplished by this technique, thereby yielding metagenomics. These techniques incorporate beginning with the entire metagenome examining, trailed by refinement, partition, and sequencing and lastly information investigation and elucidation. Particularly, the sequencing innovation is experiencing fast improvement, as it gives wide and top to bottom perspectives on metagenomics, and now it is extensively named as high-throughput sequencing (HTS) or cutting-edge sequencing technology. HTS methods incorporate the utilization of the AB SOLiD System (Life Technologies), the HiSeq 2000 (Illumina), and the 454 Genome Sequencer (Roche Diagnostics) (Yergeau et al. 2014). Besides, other propelled methods, for example, DNA/RNA-­ SIP and DNA arrays (PhyloChip and practical quality exhibits), likewise have prospective highlights in the examination of microbiomes, mostly their useful parts (Uhlik et al. 2013). At present, there is a change from metagenomics to metatranscriptomics, as the latter helps in understanding the numerous microbial functions and structure (Turner et al. 2013). In the metatranscriptomics approach, complementary DNA analysis aligned with quantitative reverse transcription-PCR and RNA-SIP explored the microbial functionality associated with the soil and rhizosphere (Uhlik et al. 2013). RNASIP significantly is used to crack the complexity in interactions especially between root-­derived carbon and microbiome so as to provide sequence as first and second utilizers of carbon within the microbiome. This method is dissimilar to DNA-SIP because it provides higher amounts of labeling and does not rely on cell multiplication. Challenges coming with these cutting-edge innovations include choosing either mRNA or rRNA alone and accomplishing more extensive inclusion of environmental RNA pool that gives naturally vital information through the sequencing. Peiffer et al. (2013) demonstrated noteworthy community contrasts among 27 maize innate lines (a genetic variant of a single species) with a normal enhanced population in the maize rhizosphere. Metaproteomics, on the other hand, has a different approach as it focuses on the dynamic function of the phytobiome and extracts samples of metaproteome and performs peptide fingerprinting by mass spectrometry (Kolmeder and de Vos 2014; Lakshmanan et  al. 2014). Using metagenomic and metaproteomic (existing and future) information is an essential process-driven methodology and should be supplemented by different strategies to decide the diversity and functional relatedness of the rhizospheric microbiome (Keiblinger et al. 2012). Molecular methods (molecular fingerprinting) and plate count anomaly (culture-­dependent methods) demonstrate the entire bacteria community structure (Amann et al. 1995). Therefore, both approaches are utilized, for thoughtful knowledge of separate classification and communication with host plants. DiniAndreote and van Elsas (2013) have, however, stressed the present need for a change in outlook from HTS (or comprehensive endeavors) to investigations of basic studies.

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3.3

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 tructural and Compositional Factors S in Plant-­Associated Microbial Network

3.3.1 Plant-Associated Bacterial and Archaeal Microbiomes Plant-associated bacterial population detected on plants does not look arbitrary; relatively numerous components participate in controlling the structure of microbiomes such as soil type (Lundberg et al. 2012), plant compartment (Leff et al. 2015), host genotype/species (Tkacz et al. 2015), plant invulnerable framework (Horton et al. 2014), plant attribute variety/developmental stage (Donn et al. 2015), and residence time/season (Shi et  al. 2015). Hacquard et  al. (2015) described that Proteobacteria, Actinobacteria, and Bacteroidetes are the major bacterial phyla that exist in both substrata such as above- and belowground plant tissues, and they influence the plant metabolism. Broad cover among root- and leaf-related network individuals has been portrayed at OTU (operational taxonomic unit) level determination in different plants such as Arabidopsis thaliana, wild mustard, grapevine, and agave (Wagner et  al. 2016), and microbiota reconstitution experiments with germ-free A. thaliana approved that root- and leaf-related bacterial networks have reciprocal relocation. Regardless of the conspicuous elementary uniformities saw between A. thaliana leaf- and root-related bacterial networks, it is observed that related microbiota individuals are particular and adjusted to their separate related plant organs (Bai et al. 2015). Among all phytobiomes, the nonpathogenic segregation of archaea has been depicted. The plant endophytic archaeal taxa of the phyla Thaumarchaeota, Crenarchaeota, and Euryarchaeota have plant-associated functional significance (Müller et al. 2015).

3.3.2 The Fungal Microbiota of Plants Ascomycota and Basidiomycota are two noteworthy phyla that colonize both aboveand belowground plant tissues (Hardoim et al. 2015). In roots, even though arbuscular (Glomeromycota phylum) and ectomycorrhizal growths have been for the most part contemplated, ongoing network profiling information demonstrates that other endophytic organisms too make up for root microbiota (Toju et al. 2013). The structure of fungal communities on plants relies upon different kinds of soil, plant parts, plant genotypes, or seasons (Coince et al. 2014) and is subjected to stochastic variations (Wang et  al. 2013) and reacts distinctively to ecological elements (Thomson et al. 2015). Thus, mostly dispersal restriction and atmosphere clarify the worldwide biogeographic conveyance of growths and have been recommended to compel contagious dispersal, supporting high endemism in parasitic populaces (Talbot et al. 2014). Steady with that, the synchronous examination of both contagious and bacterial networks related to plants recommended a more prominent significance of biogeography for organizing parasitic networks contrasted with bacterial networks (Hacquard. 2016). Regardless of using molecular markers such as 16S rRNA and ITS, their loci need to be elucidated (Peay et al. 2016).

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Recently, Yunshi et  al. (2018) quantified the prokaryotic and fungal groups within the phyllosphere and rhizosphere of six spruce (Picea spp.) tree species through illumine amplicon sequencing. In brief, this microbial quantification experiment is performed in a common garden, and linkages among phenotypic characters of their plant hosts and bacterial/archaeal and fungal community are analyzed. Correlation results among plant microbiome and different phenotypic characters of host plants (such as leaf morphology, water content, water storage ability, dry biomass, nitrogen, etc.) which suggests that plant genotype played a significant role to shape its microbiota by improving plant phenotypes.

3.3.3 P  lant-Associated Protists: The Outcasted Fraction of the Plant Microbiota Protists are a vital constituent of the soil microbiome, and method progresses now extended to our thoughts of the real taxonomic and efficient diversity of soil protists. The Stramenopiles-Alveolata-Rhizaria (SAR) group is known as a large group of plant-associated protists (Ruggiero et al. 2015) and especially those having a place with the Oomycota (Stramenopiles) and Cercozoa (Rhizaria) lineage. Inside Oomycota, a couple of individuals having a place with the genera Peronospora, Phytophthora, Pythium (and other wool buildup genera), or Albugo frequently exist in the plant roots or leaves (Agler et al. 2016). Root colonization by oomycetes (i.e., Pythium oligandrum) provides positive benefits to the host (Van Buyten and Hofte 2013). Even though plant tissue-associated oomycete network profiling stays scanty, an exceptionally low decent variety is demonstrated with individuals from the Pythiaceae family being the most spoken about to be present on plant tissues (Sapp et al. 2018). Inside Cercozoa, one of the prevailing protistan bunches in biological systems, network profiling information uncovered a surprisingly high diversity in plant roots and leaves (Ploch et al. 2016), also giving a piece of strong evidence that indicates the plant stress tolerance and metabolic behavioral changes governed by special community structure. Thus, Oomycota and Cercozoa individuals are significantly important for holobiont wellness. Recent reports concluded that plant microbe linkages are outlined well under the evolutionary measure and it helps to unlock the complex interactions of plant and microbes in more depth, and plant-­ microbe or plant bacterial interaction is new as compared to the bacterial and other kingdom interactions (Lücking et al. 2009; Hassani et al. 2018).

3.4

Microbial Currency: Exudates

Plants and microbes release certain chemicals called exudates, which help them to communicate with each other and to accelerate the disease tolerance against biotic and abiotic factors, stabilize the plant and microbial growth during nutrient scarcity, and remediate the toxic elements. Microbes utilized exudates as a food source, particularly carbon and other acids. This section discussed the two-way interaction of

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plant and microbial exudate that is influenced by plant and microbial metabolism. Huang et al. (2014) reported the significance of plant root exudates to regulate the microbial structure in the plant rhizosphere that is influenced by plant variety, growth stages, disease-suppressive soils, root exudate composition, and plant hormone signaling. Plant-microbe interaction is a complex system that is mediated by numerous compounds, and these compounds are released under specific conditions. These compounds play an indispensable role to shape the microbial community and unified the microbes and their functions up to species level. For example, legumes and rhizobia symbiosis is  signaled by flavonoids, plant mycorrhizal association is  stimulated by strigolactones, malic acid regulates the quorum sensing (QS) of plant microbial helpers and major chemoattractants of microbes such as sugars and amino acids attract the beneficial microbial niches toward the plant roots to protect the plant against the multiple stresses. However, various protein molecules are released from the root in the rhizosphere that are less explored to understand their mechanism in plant fitness. Besides, root exudates played intermediate role in several other interactions such as plant attract the nematodes, and these nematodes are the vectors of rhizobia that enhanced the nodulation of root to fix the nitrogen, plant nodulation efficiency enhanced by the interaction of rhizobia with PGPR and arbuscular mycorrhiza (Huang et al. 2014). A multitude of rhizospheric interactions is mediated by root exudates, which are depicted in Fig. 3.1.

Fig. 3.1  The complex plant microbe system of rhizosphere that is mediated by plant root exudates. Root exudates improve plant health status directly and indirectly as well

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3.4.1 Plant Uptake and Release Plant exudate components and assembly are specific to plant species and incorporate high-molecular-weight particles (e.g., sugar molecules, proteins, and fatty acid) and low-molecular-weight signaling molecules (e.g., natural compounds, metabolites, and amino acids) (Badri and Vivanco 2009). Jaeger et al. (1999) reported that plant root exudate contains sugar molecules and amino acids that help bacteria and other microbes to attract toward the plant root. Exudates assist numerous jobs such as stimulate the antagonism, allelopathic particles, and pathogen/herbivore safeguards. A large number of these exudates likewise fill in as a vitality hotspot for the microbiome; prokaryotes can use plant exudates as nutrient sources. For instance, grass Sorghum halepense excretes the exudate sorgoleone from root hairs having allelopathic properties (Kagan et al. 2003) which can be used as microbial nutrients (Gimsing et al. 2009). The different elements of plant exudate repeat the significance it fills in as numerous monetary forms of the phytobiome. Roots participate in taking up the nutrients and signaling molecules from the rhizosphere while at the same time saving these supplements and concoction signaling molecules into this equivalent space required for evoking defense reactions. Terpenoids, flavonoids, and isoflavonoids contain a large number of the plant’s antimicrobial barriers. Isoprenoids being the most diverse primary metabolite is required to control cellular processes such as photosynthesis (as phytopigments) and seed growth stimulation (as gibberellic and abscisic acids), and allelopathic molecules also protect the plants from the pathogens (Hardoim et al. 2008).

3.4.2 Microbial Uptake/Release Nitrogen fixation requires a constant need for rhizobium-legume symbiosis inside the biosphere. The ability of this methodology to enhance agricultural yield has produced attention in knowledge to manipulate this process for better use. A number of the study approaches were procured inside the examiner of rhizobia, and the precise knowledge collected from these numerous tools is used to focus on the genome- and systems-level procedures (diCenzo et al. 2019). Exudates are essential methods for correspondence within the environment for the microbial network. The uptake of exudates such as sugars, organic, and amino acids has been a noteworthy focal point of many years of research in a microbial environment utilizing different estimations of respiration or carbon substrate use measures, for example, those utilizing ECO MicroPlates™ (Biolog®). Microbial community behaves according to expanded or diminished centralizations of promptly accessible supplements that require insignificant vitality to absorb. Moreno et al. (2009) reported that a PGPB Pseudomonas putida KT2440 utilized amino acids and sugar that is concluded by the identification of proteins that regulate the amino acid and sugar uptake. The microbiome of rhizosphere has a perplexing task in nutrient cycling and includes a horde of nutrient transformations in soils. Microorganisms act as a catalyst for chemical changes in the soil during biogeochemical cycling. These changes plant

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supplement (N and P) uptake, soluble metal (Ca2+, Mg2+, K+, and Na+) uptake, and micronutrient uptake (Zn2+, Fe2/3+, Cu+, and Mn2+) (Stevenson and Cole. 1999). Nitrogen-fixing prokaryotes played a vital role to fix nitrogen gas (N2) into ammonia (NH3), and this method helps the plants. Howard and Rees (1996) reported that physiological and genetic drivers N2-fixing prokaryotes have a highly conserved protein complex that is nitrogenase, and it is used to assess the abundance of N2-fixers in diverse ecological zones (Zehr et al. 2003). Specific bacterial metabolites worked as important plant hormones, for example, indole-3-acidic corrosive (IAA) engaged with managing plant hormone flagging (e.g., 1-aminocyclopropane-­1-carboxylate (ACC) deaminase). These hormone flagging particles can advance plant development. When wheat is inoculated with rhizosphere bacteria expressing ACC deaminase activity, expanded root improvement, and consequently expanded nutrient uptake, has been recorded (Shaharoona et al. 2008; Honma and Shimomura. 1978). ACC deaminase-producing bacteria manage the ethylene production in the plant, in this manner limiting effects of different ecological anxieties, which typically trigger expanded ethylene generation (Hardoim et al. 2008). Microbial exudates involve a significant part of antimicrobial and antifungal compounds. Several prokaryotic and eukaryotic microorganisms are able to secrete or discharge antimicrobial substances, but among all very few are cultivable (Piel 2011); due to this to understand the complex functions of these substances, metatranscriptomics and metabolomics tools need to be applied. It is found that 35% of Escherichia coli strains produce the antimicrobial compound known as calcium. The discoveries bolster the theory that antimicrobial cooperations inside microbial networks serve to look after diversity; this thought was created utilizing recreation models (Czaran et al. 2002). Notwithstanding oozing antimicrobials that encourage plant resistance, microorganisms additionally release low-molecular-weight compounds to the plants, and plant sensors identify the microbes as a pathogen or beneficial and then trigger the reaction (Boller and He 2009). In this way, microbial metabolites can act straightforwardly on different microorganisms inside the microbiome in suppressive components or can act specifically on the plant to revitalize secure reactions, regularly activating plant exudation. As modern biotechnological tools improve our knowledge to measure these microbial metabolites in the soil matrix, multiple functions of the same microbiological substances are discovered.

3.5

 cological Considerations for Utilizing Plant’s Benefits E in the Farmer’s Field

An effective microbial inoculant needs to attack the pathogens and survive in varying abiotic conditions, also to set up good cooperation with the host that incorporates molecular passivity with the plant resistant framework. All through the developing season, microbial network experiences progression in both over the ground and subterranean (Edwards et  al. 2015; (Copeland et  al. 2015) portions of the plant. Along these lines, regardless of whether PGP inoculants colonize the plant at first,

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their constancy after some time isn’t ensured. Estimating the determination of bacterial inoculants in the soil presents technical difficulties, as the inoculant should be distinguished from a complex network. Strategies such as culture-based count utilizing re-separation of antibiotic-resistant inoculants or culture-­autonomous estimation of relative bounty of the inoculant’s 16S rRNA quality in the soil, by means of DGGE (Schreiter et al. 2014), amplicon sequencing (Haney et al. 2015), or metagenomic sequencing (Krober et  al. 2014), are used to determine the persistence of microbes. Ecological components impacting root exudate organization and amount include raised dimensions of CO2, dry season, and nutrient deprivation (especially nitrogen and phosphorus). Increased carbon allocated in roots is observed in CO2-fertilization experiments, resulting in shifts in exudate composition and concentration that differ with plant species (Cheng and Gershenson 2007). These species-explicit effects can result in increased yield, in no net profitability increment, or can be unfavorable to plant development and generation. For example, positive biomass reactions in rye and clover to CO2 preparation were observed, while maize demonstrated no net biomass advantage (Phillips et  al. 2006). Be that as it may, maize showed expanded exudation of a few amino acids under CO2 treatment. These discoveries are not amazing thinking about that the C4 photosynthetic pathway encourages development under elevated amounts of CO2; in any case, the effects of expanded arrival of amino acids into the rhizosphere by the C4 grass (maize) may assume a job in a large number of criticisms between different plants and organisms (Klironomos 2002).

3.5.1 Impact on Plant Functions Plants participate in nutrient exchange and exudate correspondence depending on the molecule and energy required for the plant (alone or through help from the microbiome) to acquire or release exudate currency. An active transport system using ATP-restricting tape transporter participates in root exudation creation and fixation (Badri et al. 2009). Low-molecular-weight particles such as amino acids can be discharged through membrane diffusion or through protein channels (Badri and Vivanco 2009). Plants utilize those microbes which can communicate with increased levels of N-acyl-L-homoserine lactones. AHL-degrading enzymes in the presence of a pathogen subsequently suppress gene expression of pathogens (Reading and Sperandio 2006). Plants in the same manner also help in AHL degradation inside the microbiome (Teplitski et al. 2000). Fluorescent pseudomonads which are fundamental to the rhizosphere of the different clusters of the plant are used to deliver the antimicrobials 2,4-diacetyl phloroglucinol (2,4-DAPG) and phenazine (Phz) derivatives (Mavrodi et al. 2011). These antimicrobials are of wide range and act against a number of plant pathogens that are contagious leading to their suppression (Raaijmakers et al. 2009). 2,4-DAPG and Phz derivatives are evident in the rhizosphere and are associated with the suppression of disease in wheat called as

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take-all in wheat. These plant hormones administrate the plant performance and its marking abilities to adjust to exudate profiles and enhance the plant’s immunity (Doornbos et al. 2012). Most of the microorganisms are capable of producing and controlling the majority of plant hormones (Friesen et al. 2011), thereby modifying plant physiological pathways. In plant rhizospheres, 80% of bacterial taxa accounts for IAA production (Loper and Schroth 1986). In plants, root development is accelerated with a low concentration of IAA (Glick 1999), while its high concentration represses plant’s development, hence making plants prone to pathogen’s attack (Sarwar and Kremer 1995). An example of this is seen in Sorghum halepense; microbes of the invasive grass secrete high concentrations of IAA in contrast to other prokaryotes that secrete lower levels of IAA (Rout et al. 2013). Environmental stress and plant phenology drive the changes in plants that need to increase or decrease the hormones. PGPB are competent cells having multiple genes required for plant-microbial association (Hardoim et al. 2008). Yield expansion, organic methodologies, intercropping, and other cultural practices are utilized for possible farming production. New strategies are formulated to modulate the plant microbiome in an ideal course (Fig.  3.1). Distinctive microbiota is induced by diverse agro-management in viticulture (natural, biodynamic, or biodynamic with green compost) (Longa et  al. 2017). It is observed that in an integrated management system, soil has diminished bacterial species richness as compared to organic management, even though microbial composition was similar to organically and biodynamically managed soils (Hendgen et al. 2018).

3.5.2 Impact on Bacterial Functions Microbiome present in the rhizosphere possesses varied phenotypic expressions due to root exudates. Inhabitant microflora of plants perform different functions such as chemotaxis, stress tolerance (Amador et al. 2010), polychlorinated biphenyl degradation (Toussaint et al. 2012), modulation of genes involved in competence and sporulation (Mader et  al. 2002), and biofilm formation on plant roots (Rudrappa et al. 2008). Plant exudates such as terpenoids, flavonoids, and isoflavonoids protect and control the internal structure of plants and outward surface of roots from microbial inhabitant (Hardoim et al. 2008). Microbiome symbionts can be epiphytes or endophytes, which survive for a short growth period and may encompass not only the pathogens but plant growth-promoting microbes using a mechanism of hormone signaling. Organic farming impacts the community composition on soil and roots of winter wheat (Hartman et al. 2018). The structure of bacterial communities is taken care of by tillage. Root bacteria respond to management types, whereas fungal communities respond to both. Different agricultural practices are parameters in affecting the microbial structure with differences in soil, roots, bacteria, and fungi and hence bringing around 10% of the variation in microbial communities.

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Formation of Biofilm

Microbial communities act as a unit and secrete polymeric substances to produce a network known as biofilms (Stoodley et al. 2002). Microbes, when present in a biofilm as consortia, are highly protected from their competitor, antimicrobial agents, enzyme degradation, and acquisition of new genes through horizontal gene transfer (Van Acker et al. 2014; Nadell et al. 2009; Zhang et al. 2014). Enterobacter spp., a root-occupying bacterial endophyte, when forming a biofilm, inhibits the entry of root-colonizing pathogen Fusarium graminearum (Mousa et al. 2016). Bacteria commonly produce biofilms on fungi, but it is rarely seen on the hyphae of ascomycete fungi. An example of this is seen in Pseudomonas fluorescens BBc6 which formulates biofilm on the hyphal region of the ectomycorrhiza Laccaría bicolor specifically at its root tip, thereby establishing ectomycorrhizal beneficial symbiosis and promoting bacterial biofilm on fungal host surfaces (Guennoc et al. 2017).

3.7

Molecular Communications

The mechanism of quorum sensing is used by microbes to sense their counterparts. Gram-negative microorganism secretes signaling molecule N-acyl-l-homoserine lactone (AHL) to screen out their populace densities (Eberl 1999). Regulation and secretion of signaling molecules are evident in Saccharomyces cerevisiae and Candida albicans (human fungal pathogens) that secrete farnesol to control filamentation (Oh et al. 2001), constrain biofilm formation, and activate oxidative stress responses or drug efflux (Sharma and Prasad 2011). Quorum sensing mechanisms are not defined thoroughly for plant-associated fungi. Signaling compounds such as volatile organic compounds (VOCs), oxalic acid, trehalose, glucose, or thiamine accelerate fungal bacterial associations (Schmidt et al. 2016).

3.8

Ecology of the Microbiome

The plant microbiome is localized in three different regions, namely, rhizosphere, endosphere, and phyllosphere (Hirsch and Mauchline 2012). Rhizosphere presents a microbial community in requirement with plant metabolism; endosphere presents those microorganisms which interact with host closely and inhabit inner part of plant tissues asymptomatically (Hardoim et al. 2008); phyllosphere, on the contrary, is composed of those microbes which inhabit plant surfaces (Lambais et al. 2006). Irrespective of different plant habitats, specific microbes are present in all, also known as “keystone” species which interact with other microbes within the networks and affect the microbial structure (Bakker et al. (2014). Rhizosphere and endosphere account for root microbiome that was key for the advancement of land plants and underlay crucial ecosystem processes. It is reported that nearly 30 angiosperm species affect root bacterial diversity and composition (Fitzpatrick et  al. 2018). A competitive interaction gets affected when there is a

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similarity in root microbiomes between hosts among plant species. Climatic parameters such as drought affect the root microbiome composition, by elevating the Actinobacteria population. In the endosphere, Streptomyces are associated with host drought tolerance influencing drought response crosswise over host plant species bringing host-specific changes.

3.8.1 Rhizosphere and Rhizoplane Plant health is influenced by the rhizosphere using next-generation and third-­ generation technologies (Hiltner 1904). Rhizospheric soil shows a significant difference in contrast to bulk soil due to abiotic and biotic stresses impacted by the atmosphere. Properties such as higher water holding capacity, expanded nutrient availability, and diverse microbial biomass mark its importance than bulk soil (Schade and Hobbie 2005). Spatiotemporal movements are observed in the rhizosphere microbiome (Kaplan et  al. 2013); however, it is still to affirm how much abiotic stresses impact the microbiomes. Protection from a wide range of pathogens both aboveground and belowground is provided by microbiomes. For example, induction of systemic resistance (ISR) is initiated where jasmonic acid-inducible genes are secreted in leaves (Pineda et al. 2010).

3.8.2 Epiphytes and Endophytes The epiphyte and endophyte microbial communities in root involve the acknowledgment and selection of those microbiomes that establish a homeostatic association with the plant. Technologies such as metabolomics and metatranscriptomics are used to observe microbial members that colonize in adherent (epiphytic) or internal (endophytic) parts of plants. Microbes colonize the outside root surfaces. For instance, secondary metabolite root exudates were released due to an ISR response in maize that appoints PGPB P. putida, based on chemotaxis inclinations (Neal et al. 2012). Plant chemical exudate is secreted, and valuable PGPB is selected in a plant-­ mediated reaction as observed in tomato, where natural acids are the major chemotactic operator (De Weert et al. 2002), while in rice, amino acids serve the purpose (Bacilio-Jimenez et al. 2003). Root microbes that laid distinctive qualities such as that code for the sort IV pilus and twitching motility (Bohm et al. 2007), isoflavonoid efflux siphon (Palumbo et al. 1998), and DNA improvements influence colony aggregation (Dekkers et al. 1998). Endophytes are inhabitant to both wild and domesticated crops including intrusive species (Compant et  al. 2008; Rout and Chrzanowski 2009). Biotechnology and agriculture ensure to utilize plant developing qualities of microbiomes as seen in phosphate-solubilizing Bacillus strains, where apart from secreting protein ACC deaminase, these also show plant development advancements (Baig et  al. 2012). Thus, a microbiome serves a double attribute working together with mycorrhizal parasites to improve plant development advancement (Zaidi and Khan 2005).

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Plant phenology correlates with endophyte microbiome composition shifts (van Overbeek and van Elsas 2008) which further depends upon colonization and similarity (Hardoim et al. 2008). This collaboration inclines more toward mutualism than parasitism. Most of known plant endophytes and epiphytes are horizontally transmitted (Friesen et  al. 2011). This empowers host-to-host exchange of endosymbionts without the association of plant sexual reproduction. Endophytes also show vertical transmission depending upon host wellness and present more host benefits than horizontal transmission (Clay and Schardl 2002; Sachs et al. 2004). But the environmental hypothesis proposes that the presence of an accessible host allows for horizontally transmitted life forms. It is observed that horizontally transmitted endophytes were positively related to plant thickness reliance, while vertically transmitted endophytes did not demonstrate this pattern (Rudgers et al. 2009).

3.8.3 Phyllosphere Region Phyllosphere is regarded as a third segment of the plant microbiome that colonizes the outside region of the external area of plant tissues specifically when describing the leaf surface (Vorholt 2012). The microbiomes in the phyllosphere perform nitrogen fixation, securing plants against attacking pathogens and biosynthesizing phytohormones (Kishore et al. 2005). These can be beneficial in carbon sequestration (Bulgarelli et  al. 2013), and they can also participate in sustainable agricultural practices. Fungi (filamentous and yeasts), bacteria, and algae make phyllosphere network, and at lower frequencies, protozoa and nematodes are seen (Lindow and Brandl 2003). The bacterial population is the most abundant group of microorganisms present in the phyllosphere at numbers ranging from 105 to 107 cells for each cm2 (Andrews and Harris 2000). These microbes can thrive in harsh environmental conditions such as limited availability of nutrients and variable conditions of humidity, UV radiation, pH, and temperature (Andrews and Harris 2000). The phyllosphere community is created with the help of various hotspots as air, soil, and water (Bulgarelli et  al. 2013). Agricultural plants also show specificity to phyllosphere microbiomes as seen in beans, cucumber, grasses, lettuce, and maize (Rastogi et al. 2012). Plant genotype plays a significant effect on the composition of phyllosphere microbiomes (Bokulich et al. 2014). The microbial population shows intraspecific variations in its composition which are due to nutritional heterogeneity observed in regions on the leaf surface where heterogeneous carbon sources such as glucose, fructose, and sucrose are utilized near the stomata and surface appendages (Vorholt 2012). At times, this heterogeneity is observed when microbial cells aggregate to form a biofilm and hence defending themselves from unfavorable conditions (Lindow and Brandl 2003). Proteobacteria, Actinobacteria, Bacteroidetes, and Firmicutes are major phyla that account for the microbial community in the phyllosphere region (Vorholt 2012). Hence, this core is accepted to be made out of individuals exhibiting a co-developmental history with plant species, with the host physiology being complementary to the features found inside the microbial cells. Microbes such as protists largely act as

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predators on the bacterial community (Flues et al. 2017). Environmental conditions such as low nutrients, high UV, changing temperature, and humidity help in selecting consistent biological traits and low functional diversity at the community level for phyllosphere microbiomes as observed in next-­generation sequencing (Lambais et al. 2017). The phyllosphere is dominated by oxygen-consuming organoheterotrophs, and metabolic diversity exists with regard to utilizable carbon compounds.

3.9

 ompetitive Interactions Among Plant C Microbiota Members

Plant microbiomes show competitive behavior with closely or distantly related microbiota and affect microbial structure, its stability, and homeostasis.

3.9.1 Resource Competition Microorganisms utilize limited resources and therefore compete indirectly with other microbes. For example, using advanced techniques, microorganisms sequestrate iron using the emission of siderophores, thereby affecting the growth of the opponent microbes present in their niche (Little et al. 2008). When advantageous Pseudomonas spp. secrete iron-chelating molecules, it suppresses the disease caused by fungal pathogens indicating that nutrient sequestration is a trait of biocontrol agents to outpower pathogens (Mercado-Blanco and Bakker 2007). In tomato plants, resource competition is said to be an essential factor connecting the bacterial network and pathogen attack on plants (Wei et al. 2015). In resource competition, individual microbes in a group share resources, but the ones who use the resources in an uncooperative can evade paying the price of cooperation while reaping the benefits of utilizing the resource, thereby increasing their fitness (Riehl and Frederickson 2016) and bringing the situation of distress to the commons. Nitrogen-­ deficient soil could harbor plants with rhizosphere having microbes that can capture nutrients for their usage. For instance, actively growing roots could signal for microorganisms that are capable of producing extracellular enzymes releasing nitrogen bound in soil organic matter (Lemanceau et al. 2017). In prokaryotes, mineralization processes are density-dependent and need a quorum of producers to sufficiently enter key nutrients in the soil. Such producers are taxonomically diverse microbiota that can biosynthetically produce the specific enzymes which are secreted into the soil. In this scenario, selection in the rhizosphere could favor microhabitats to promote coordinated group behaviors that enhance plant access to nitrogen or phosphorus upon cell turnover, while the microorganisms benefit from having an abundant supply of carbon and other nutrients from plant roots (Fig. 3.1). Phosphorous is also made available to plants using microbial taxa which could mobilize phosphorus in the soil via the production of extracellular compounds (Alori et al. 2017). Iron is an important plant nutrient which can be obtained through the production of siderophores (Radzki et al. 2013).

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3.9.2 Contact-Dependent Competition Plant microbiome participates in direct antagonistic cooperations interceded by the bacterial type VI secretion framework, a molecular weapon used by certain microscopic organisms (generally Proteobacteria) to convey effectors/toxins into both eukaryotic and prokaryotic cells (Records 2011). A few examples of contact-­ dependent competition are discussed as in the case of the plant pathogen Agrobacterium tumefaciens that utilizes a puncturing type VI secretion system to convey DNase effectors upon contact with a bacterial competitor in vitro and on the leaves of Nicotiana benthamiana. Moreover, the bacterial kind III secretion system can also be used in Burkholderia rhizoxinica, which uses this mechanism to control the productivity of its beneficial interaction with the contagious host, Rhizopus microspores. Physical parameters bring a change in plant-associated microbes. Soil condition (organic matter, nitrogen, and moisture content) identification helps in changing the macrophage activation potential of Echinacea purpurea and determining these changes in activity that relates to the shifts (Haron et al. 2019). Increasing soil organic matter in the root extracts of E. purpurea may increase the macrophage activation. Bacterial communities also differed significantly between root materials having varying levels of organic matter. The activity of E. purpurea roots is changed by the soil’s organic matter level. Use of bacterial preparation (e.g., probiotics) is reported to impact human health; similarly, Echinacea too shows therapeutic effects and is impacted by development conditions that change its related bacterial community (Haron et al. 2019).

3.9.3 Antimicrobial Compound Secretion Various plant-related microorganisms appeared to emit chemical compounds that stifle the development of microbial rivals (Raaijmakers and Mazzola 2012). Filamentous eukaryotes are outstanding in delivering a large number of antifungal activity of secondary metabolites that have a low molecular weight spotted against phylogenetically distinct organisms (e.g., acetylgliotoxin and hyalodendrin) (Coleman et al. 2011). The secondary metabolites so obtained become activated in co-culture and remained inactive in pure culture. Netzker et al. (2015) indicate their specific role in competitive interactions. Antagonistic collaborations among microscopic organisms have been reported to be imperative in the organizing of soil-, coral-, or plant-related bacterial networks (Maida et al. 2016). Strikingly, the investigation of adversarial collaborations among bacterial segregates from the rhizosphere, the roots, and the phyllosphere of the healing plant Echinacea purpurea proposes that plant-related microorganisms compete against one another through the discharge of antimicrobials (Maida et al. 2016). The microbiome related to plants has a robust influence on their strength and yield. The bacterial pathogen, Candidatus Liberibacter asiaticus (Las), causes Huanglongbing (HLB) disease and lives inside the phloem of citrus plants, including the root system. It has been proposed that Las negatively affects citrus microbiome. At the

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same time, the natural microbial flora of citrus also impacts the association between Las and citrus (Riera et  al. 2017), i.e., two bacteria closely related to Las Agrobacterium tumefaciens and Sinorhizobium meliloti were found. Among them, Burkholderia metallica strain A53 and Burkholderia territorii strain A63 are within the β-proteobacteria class, whereas Pseudomonas granadensis strain 100 and Pseudomonas geniculata strain 95 are within the γ-proteobacteria class. It was observed that four bacterial strains Burkholderia territorii A63, Burkholderia metallica A53, Pseudomonas geniculate 95, and Bacillus pumilus 104 showed antagonistic action against the pathogen Phytophthora nicotianae (citrus root) on the basis of dual culture assays. Some of the antimicrobial-producing strains, Burkholderia metallica A53 and Burkholderia territorii stress A63, from a mandarin rhizosphere, belong to the Burkholderia cepacia complex (BCC) and its agricultural applications are restricted because of its high risk to human health (Depoorter et al. 2016). It remains to be determined whether Burkholderia metallica strain A53 and Burkholderia territorii strain A63 can cause human diseases. Both Burkholderia metallica A53 and Burkholderia territorii strain A63 can modulate citrus immune system beneath greenhouse situations while applied as a soil drench. Additionally, the Burkholderiaceae family changed into determined to be key taxa within the citrus microbiome of healthy trees in comparison to that of HLB-symptomatic trees in the discipline (Zhang et al. 2017).

3.9.4 Predation Bacterial mycophagy comprises of microscopic organisms’ capacity to effectively develop at the expense of living contagious hyphae (De Boer et  al. 2004). Mycophagous microbes colonize saprotrophic rhizosphere parasites and feed as auxiliary consumers on root-determined carbon (Rudnick et al. 2015). Some oomycetal species of family Trichoderma or Pythium can parasite or irritate other growths or oomycetes and can be utilized as biocontrol operators (Benitez et al. 2004). Root-­ related bacteria can prey on other microscopic organisms as described for Bdellovibrio spp. Protist predation on microscopic organisms is also well studied, and recent microbiota reconstitution tests in microcosm demonstrate a reasonable impact of Cercomonads (Rhizaria: Cercozoa) on the structure and the capacity of the leaf microbiota (Flues et al. 2017). Their results show that Alphaproteobacteria and Betaproteobacteria are less impervious to grazing and that predation rebuilds the bacterial system in leaves and impacts bacterial metabolic center capacities. Microbial assortment related to aphid inhabitants was characterized at species and intraspecies scales using a methodological structure (Guyomar et al. 2018). Utilizing this approach, on metagenomics read sets, high genomic diversity in different symbiont taxa can be uncovered in both between and within their hosts. The complete functional diversity related with host and microbiota was the first time it can be accessed using metatranscriptomics datasets which also helps in isolating the transcriptome of each member of the holobiont (Meng et al. 2018).

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3.9.5 G  enetic Management of Valuable Plant-Microbe Interactions Host hereditary qualities add to plant microbiome assembly. Plants identify microorganisms through pattern recognition pattern that binds to the microbe-associated molecular pattern (MAMPs), setting off a basal barrier adequate to stop the development of most pathogenic organisms (Böhm et  al. 2014). Plants can probably separate pathogens from nonpathogens and react by opposing microbial development, overlooking it, or effectively supporting it on or inside plant tissues. The transcriptional reaction of Arabidopsis leaves varies when vaccinated with various nonpathogenic individuals from its regular microbiota (Böhm et al. 2014). While Methylobacterium extorquens actuates no transcriptional reaction, Sphingomonas melonis initiates the defense-related genes that somewhat cover with those activated by the pathogen Pseudomonas syringae DC3000. This characterizes a mechanism of plant defense priming (Martinez-Medina et al. 2016) driven by the plant microbiome. The reaction example to nonpathogenic microorganisms can vary both crosswise over plant species (Ofek-Lalzar et al. 2014) and crosswise over promotions inside a single species (Haney et al. 2015). While some Arabidopsis accessions are colonized by and build up a valuable association with Pseudomonas fluorescens, different promotions effectively restrain the development of similar strains in their foundations. Given the basic capacity of defense phytohormones in the invulnerable plant framework, it is not astonishing that the plant microbiome organization is impacted by defense phytohormone flagging. Tests by a set of mutants with transformed protection phytohormone synthesis and notion stated that salicylic acid and salicylic acid-mediated events have an effect on the root microbiome composition at multiple taxonomic levels (Lebeis et al. 2015). The plant microbiome structure changes upon infection (Agler et al. 2016). Antifungal characteristics are enhanced in barley following infection with Fusarium graminearum, conceivably using changes in exudate arrangement (Dudenhöffer et al. 2016). An investigation of tomato plants tested with the pathogen Ralstonia solanacearum uncovered that the root exudation profile changed upon pathogen infection, expanding the discharge of phenolic mixes. Plant protection systems additionally sway different drivers of plant – organism cooperations, similar to plant sustenance (Hacquard et al. 2015). Present-day molecular methodologies are likewise being connected to understanding nitrogen-fixing symbioses in non-nodulating plants. Utilization of double host-organism transcriptomics depicted that the limit of a nitrogen-fixing Burkholderia strain to frame microaerobic biofilms on sugarcane roots is shown to have diminished motility and immunogenicity, trailed by metabolic adjustment to the sugar-rich plant condition. The plant does not enact an invulnerable reaction but, however, changes its root morphology and supplies the bacterium with photosynthates (Paungfoo-Lonhienne et al. 2016), a reaction pattern that is undifferentiated from the procedure of infection by BNF in legumes (Cao et al. 2017). These examples endorse that the coordination of defense and nutrition is crucial to driving microbiome characteristics.

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3.10 I mplication of the Soil Microbiome on Sustainable Agriculture and Food Security Conveying sustenance security, the way toward expanding nourishment creation, and improving nourishment quality to support populace development without trading off ecological well-being have been known as a worldwide green revolution (Gupta 2012). Sustainable agriculture improvement is expected to relieve these issues. A definitive objective of economical agribusiness, as per the US National Research Council, is to create cultivating frameworks that are gainful, beneficial, vitality saving, and environmentally solid, preserving natural materials, and that guarantee nourishment well-being and quality. This can be achieved by substituting risky agrochemicals (chemical fertilizers and pesticides) with environmentally friendly beneficial microorganisms, which could improve the sustenance of yields and animals and furthermore present protection from biotic (pathogens and pests) and abiotic (pollution and climatic change) stresses. The potential microbial segregates are detailed utilizing different natural and inorganic bearers through either solid or liquid fermentation technologies (outlined in Table 3.1). Table 3.1  Marketable products of plant growth-promoting rhizobacteria in plant health and disease management (Lakshmanan et al. 2014) Bioagent Agrobacterium radiobacter strain K1026 A. radiobacter strain K84 Azospirillum brasilense/Azotobacter chroococcum A. brasilense B. subtilis MB1600 B. subtilis strain FZB24 Bacillus chlororaphis 63-28 Bacillus cereus BPO1 Bacillus pumilus GB 34 B. pumilus QST2808 B. subtilis GB03 Bacillus amyloliquefaciens GB99 Bacillus licheniformis SB3086 Burkholderia cepacia P. fluorescens A506 Pseudomonas syringae ESC-100 Pseudomonas chlororaphis Pseudomonas cepacia Streptomyces griseovirdis K61 B. subtilis + B. amyloliquefaciens Pseudomonas spp. + Azospirillum spp.

Trade name/formulation Nogall Galltrol, Diegall Gmax Nitromax Azo-Green BaciGold, HiStick N/T, Subtilex Rhizo-Plus, Serenade, Rhapsody, Taegro, Tae-Technical AtEze Pix plus Concentrate; YieldShield Sonata ASO, Ballard Companion, System 3, Kodiak, Kodiak HB, Epic Quantum 4000 EcoGuard, Green Releaf Blue Circle, Deny, Intercept BlightBan A506, Conquer, Victus Bio-Save 10, 11, 100, 110,1000, and 10 LP Cedomon Intercept Mycostop Bio Yield BioJet

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Further improvement of microbial confines, and the plan procedure is required through broad research to present them in sustainable agricultural practices. Applications of microbial consortia are described in Table 3.2. Aside from the application of individual organisms, distinguishing sound and practically diverse microbiomes and their application for improving harvest yield poses another big challenge to meet.

3.11 Conclusions Several illustrations depict the significance of understanding the multitude of plant microbiome relations that pay to plant versatility in a specified environment. Acknowledgment of the plant microbiome as a coordinated part of the plant genome develops the environmental idea of “feedback.” Disproportional accumulation  of microbiome parasites (communicated as pathogenic impacts) prompts negative feedback, whereas the disproportional combination of microbiome mutualists stimulates positive  feedback. An enhanced information about these interactions and how changes in biodiversity affect ecosystem functions (plant yield, biogeochemical pools, and fluxes) may be a vital feature for explaining plant microbiome boom and gene expression forms. Fast microbial generation time and the prevalence of horizontal gene transfer give probable systems to the improvement of localized genetic differences, or ecotypes, to emerge because of the impacts of local  plant species and networks. As the plant-microbiome interaction unfolds, a new emerging  methodology incorporates the study  of microbial biology, microbiomes, and transcriptomes into plant genetics. The vast diversity documented in the rhizosphere microbiome is  linked with the useful genes responsible for important nutrient changes, similar to those involved in N2-fixation. The age of expansive confine accumulations and the investigation of engineered microbial networks in the mix with plant genetic properties will enable us to connect this hole and to direct reductionist, theory-driven tests in progressively complex environmental settings up to handle field tests. These developments can convert our expertise of plant-microbe interactions in nature and agriculture and could make contributions extensively to the next green revolution. The key player(s) regarding microbiome structure have not been recognized. As needs are, there is a major break in the identification of the molecular segments associated with the collaboration among the host plant and the microbial populace. Also, these ongoing microbiome examinations attempted only to distinguish its structure and multifaceted nature instead of to decide how these microbial gatherings are adjusting the plant phenome, which is basic to investigate its usage. Likewise, there would be a cross talk using signal transduction among aboveground and belowground plant tissues that can be modified by an outer biotic or abiotic stress impacting the rhizospheric microbiome.

Desiccation

Drought

Hyaloperonospora, Pseudomonas putida KT2440, Sphingomonas sp. OF178, Azospirillum brasilense Sp7, Acinetobacter sp. EMM02/unknown

Acinetobacter sp. S2 and Bacillus sp. S4, Sphingobacterium sp. S6, Enterobacter sp. S7 and Delftia sp. S8/Vitis vinifera rhizosphere and endosphere Arthrobacter nitroguajacolicus E46, Bacillus mojavensis K1, Pseudomonas frederiksbergensis A176, Arthrobacter nitroguajacolicus E46, Bacillus cereus CN2, Bacillus megaterium B55, Bacillus mojavensis K1, Pseudomonas azotoformans A70, Pseudomonas frederiksbergensis A176, Bacillus megaterium B55, Pseudomonas azotoformans A70/tobacco plants

Blue maize CAP15–1 TLAX/greenhouse pots with vermiculite

Capsicum annuum, Vitis vinifera cv. Barbera, growth chamber, greenhouse Nicotiana attenuate, field

Natural wilt disease

Ralstonia solanacearum

Phytophthora infestans

Pseudomonas syringae pv. tomato

Stress Hyaloperonospora arabidopsidis

Pseudomonas spp. CHA0, PF5, Q2–87, Q8R1-96, 1M1-96, MVP1-4, F113, Phl1C2/pea, wheat, cotton, tomato, sugar beet, tobacco

Consortia/origin of bacteria Xanthomonas sp. WCS2014-23, Stenotrophomonas sp. WCS2014113, Microbacterium sp. WCS2014-259/field soil with endemic Arabidopsis plants Bacillus megaterium SOGA_2, Curtobacterium ceanosedimentum SOGA_3, Curtobacterium sp. SOGA_6, Massilia aurea SOGA_7, Pseudomonas coleopterorum SOGA_5, 11, and 12, Pseudomonas psychrotolerans SOGA_13, Pseudomonas rhizosphaerae SOGA_14 and 19, Frigoribacterium faeni SOGA_17, Xanthomonas campestris SOGA_20/phyllosphere of field-grown tomato plants Double or triple combinations of Pseudomonas spp. R32, R47, R76, R84, S04, S19, S34, S35, S49/rhizosphere and phyllosphere of field grown potatoes

Solanum tuberosum cv. Lady Clair, cv. Victoria, cv. Bintje, leaf disks in petri dishes Lycopersicon esculentum cv. Jiangshu, greenhouse pots with soil

Plant and growth conditions Arabidopsis thaliana, growth chamber, non-sterile soil Solanum lycopersicum cv. Moneymaker, growth chamber

Table 3.2  Application of bacterial consortia (Compant et al. 2019)

de Vrieze et al. (2018) Hu et al. (2016)

Reduced fungal sporangiophore development Reduced disease severity and pathogen abundance Increase of shoot and root dry weight, plant height and plant diameter Increased fresh root, aerial biomass, and photosynthesis Less dead plants

Santhanam et al. (2015)

Molina-­ Romero et al. (2017) Rolli et al. (2015)

References Berendsen et al. (2018) Berg and Koskella (2018)

Consortia effect Less fungal spores and higher plant fresh weight Fewer pathogen DNA copies on leaf disks

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4

Plant Mycobiome: Current Research and Applications Ajit Kumar Dubedi Anal, Shalini Rai, Manvendra Singh, and Manoj Kumar Solanki

Abstract

Plant mycobiome studies are one of the leading burning aspects of the twenty-­ first century for ecological management and sustainable agricultural. A plant-­ associated fungal community plays an important role in maintaining ecological fitness by cycling organic matter and channeling nutrients across the trophic levels. Several reports highlighted the need for plant mycobiome studies for better disease management, ecological practices, and the use of eco-friendly methods for crop production. In this context, plant mycobiome revealed the effect of the fungal community on the composition of other microbial communities associated with the plant, plant growth, and plant responses against the pathogens. Fungal biodiversity, functionality, and associative interaction with other microbiome organisms and plants are revealed by high-throughput sequencing methods that broaden our view on understanding the fungal importance to plants. The present chapter discussed the modern tools and techniques utilized to study fungal diversity and community structure by the use of different kinds of OMICS approaches such as ITS rDNA gene or specific functional gene sequencing, transcriptomics, proteomics, and metabolomics. Here, the chapter focused on the current research, development of new techniques and approaches that can provide an integrative insight of the role of fungal communities in the plant A. K. D. Anal Amity Institute of Microbial Technology, Amity University, Noida, Uttar Pradesh, India S. Rai (*) Department of Biotechnology, Society of Higher Education and Practical Application (SHEPA), Varanasi, Uttar Pradesh, India M. Singh ICAR-National Research Centre on Litchi, Muzaffarpur, Bihar, India M. K. Solanki Department of Food Quality & Safety, Institute for Post-harvest and Food Sciences, The Volcani Center, Agricultural Research Organization, Rishon LeZion, Israel © Springer Nature Singapore Pte Ltd. 2020 M. K. Solanki et al. (eds.), Phytobiomes: Current Insights and Future Vistas, https://doi.org/10.1007/978-981-15-3151-4_4

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­ icrobiome. Plant mycobiome and their diversity are important to predict plant m growth and survival against the pathogen and multitrophic interactions between the organisms to identify their functional cores in regard to plant health and forecast which fungal community is likely to affect plant fitness and produce useful secondary metabolites. Keywords

Mycobiome · Sequencing technique · Plant pathogen · Biofertilizer

4.1

Introduction

The plant mycobiome represents the plant-associated fungal community that have multiple functional roles, in response to plant, ecological management, and environmental indications (Finzi et al. 2011; Pagano et al. 2017). The plant-associated fungal community is most commonly associated with both terrestrial and aquatic ecosystems by continuous degradation of organic matter and cycling nutrients across the trophic levels of the food web (Delgado-Baquerizo et al. 2013; Toju et al. 2018). These communities are cosmopolitan in different ecological habitats, such as natural soils, decaying wood, and plant material, living plants (endophytes), water-­related environments, etc. (Rai et al. 2019; Hardoim et al. 2015). Most of these fungal species are saprophytes, and they are capable to decompose complex polymers such as cellulose, chitin, and lignin by different hydrolytic enzymes (Benitez et al. 2004; Anil and Lakshmi 2010; Błaszczyk et al. 2014). Several factors, like plant host, plant density, environmental conditions, nutrient availability, and interactions with other external microbiomes (e.g., soil fungi and bacteria), are contributed to maintaining the plant mycobiome composition (Bahram et al. 2015; Nilsson et al. 2018). The plant mycobiome is usually comprised of five main functional groups of fungal communities, viz., saprotrophic, pathogenic, epiphytic, endophytic, and mycorrhizal fungi (ectomycorrhizal fungi, arbuscular mycorrhizal fungi, ericoid mycorrhizal fungi, and orchid mycorrhizal fungi) (Porras-Alfaro and Bayman 2011; Beckers et al. 2016). The plant-associated fungal community is participating in mineral conduction, carbon distribution, water acquisition, tolerance to abiotic and biotic stresses, and interplant competition (Bucher et al. 2009; Druzhinina et al. 2011; Cai et al. 2013). They applied different mechanisms, such as parasitism, stimulation of plant growth, competition for nutrients, cross-protection, microbial compound production, and induction of systemic resistance against abiotic and biotic stresses in plant mycobiome to maintain ecological fitness and fungal diversity (Kubicek et al. 2011; Porras-Alfaro and Bayman 2011; Hardoim et al. 2015; Cai et al. 2015). Several reports highlighted the increasing interest of plant mycobiome studies to explore hidden mechanisms and reshape the rhizospheric microbiome for biofertilization, which stimulates plant growth, protection from stress, parasitism, antibiosis, induced plant systemic resistance, and rhizoremediation (Ikeda et al. 2010; Hu et  al. 2018). The mycobiome research will draw new insights into plant fungi

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interaction that can help to understand the complex networking and ecological function of fungi. In this context, molecular identification revealed the cultivable and uncultivable fungal communities of mycobiome that gives information about mycobiome diversity, structure, compositions, and signaling mechanism between the host plant and associated microbiome (Bayman 2006; Chacon et al. 2007; Tellenbach et  al. 2010). However, due to limited knowledge of plant-associated mycobiome composition, diversity, and functionality, these subjects need to explore up to depth. The modern molecular approaches such as high-throughput sequencing methods and omics techniques (epigenomics, genomics, transcriptomics, proteomics, and metabolomics) are utilized to identify the function of fungal communities with plant and soil as well as with other microbes in different habitats (Bálint et al. 2016; Gohl et al. 2016; Kchouk et al. 2017; Castle et al. 2018). This chapter focuses on plant mycobiome compartments (rhizosphere, phyllosphere, and endosphere) and interactions between plants and microorganisms with major emphasis on fungal fractions of the microbiome within each compartment. The chapter discussed the significant application of plant mycobiomes to improve plant health and how artificially engineered mycobiome can help the crop to improve productivity. This study provides a summary of recent and cutting-edge techniques that can help to classify the fungal communities, their biodiversities, and plant-­ associated functions.

4.2

Plant-Associated Microbial Communities

The soil-inhabiting fungal communities play a vital role in plant health management. They suppress plant diseases through physiological restrictions of pathogen establishment in plant tissues (Mendes et al. 2011; Mukherjee et al. 2012; Classen et al. 2015) and help to convey resistance to the system against “invaders” (Pérez-­ Jaramillo et al. 2018). Several additional factors have been recognized to mycobiome in close association with plants such as ability to provide nutrient mobilization, like phosphorus solubilization and nitrogen fixation, their support in nutrient uptake from the soil, suppression of abiotic and biotic stresses, host health, and ecological fitness (Molla et  al. 2012; Oros and Naár 2017). The plant-associated microbial communities usually comprise five main functional groups of fungal communities, saprotrophic, pathogenic, epiphytic, endophytic, and mycorrhizal, which performs different functions in ecological balancing (Mendes et al. 2013). The major studied compartments of plant-associated microbial communities are established microbial cells and perform distinct functions, called rhizosphere, phyllosphere, and endosphere (Herrera et al. 2010; Porras-Alfaro and Bayman 2011).

4.2.1 Rhizosphere Fungal Microbiome Communities Lorenz Hiltner coined the term rhizosphere in 1904 (Curl and Truelove 1986), which refers to the bulk of soil surrounding the plant roots. Rhizosphere provides

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opportunities to organisms to competitively colonize plant roots by secreting root exudates, which are active carbon compounds, and uptake of mobile nutrients and water (Hartmann et al. 2008; Singh and Sharma 2012). The biodiversity and community structure of fungal communities are maintained by the coevolutionary process of rhizosphere and plant roots which perform a significant role in soil biological processes, soil carbon sequestration, and nutrient channelization through decomposed matter cycling in natural systems (Hinsinger et al. 2009; Lambers et al. 2009). The plant rhizosphere system generally enhanced the biomass and soil microorganism’s activities by releasing root exudates, which respond with chemotaxis and grow faster (Hartmann et al. 2009). The rhizosphere microbial community composition and diversity are affected by plant growth, as root exudates change during the plant’s life cycle and seasonal environment responses (Baetz and Martinoia 2014). The rhizospheric fungal communities are closely interconnected to plant health, fitness, and growth, decaying plant residues, providing nutrients by cycling minerals, and facilitating their roles in antagonizing pathogens (Ehrmann and Ritz 2014). The beneficial fungal microbes include mycorrhizal fungi (Zhang et  al. 2018; Turrini et al. 2018), Trichoderma strains (Kotasthane et al. 2015; Li et al. 2015), Penicillium sp. (Babu et al. 2015), and other endophytic fungi like Fusarium sp., Colletotrichum sp., Cladosporium sp., and Dendrobium moniliforme (Chadha et al. 2015; Shah et al. 2019) which are an indispensable component of agroecosystems. In response to microbial activities, plants fundamentally control rhizospheric fungi through the production of carbon and its derivative compounds and bioactive metabolites (Ellouze et al. 2014). Several examples are elucidating the role of fungal communities, as biocontrol, activity against pathogenic microorganisms (Kowalchuk and Veen 2004, Chapelle et al. 2016). Trichoderma is a hyper-diverse genus of rhizospheric fungal community that gained importance due to their antagonistic capability to plant pathogen by employing different mechanisms of parasitism, stimulation of plant growth, competition for nutrients, and induction of systemic resistance against abiotic and biotic stresses (Rai et al. 2016). These fungal communities positively influence plant productivity and protect the plants from oxidative stress by synthesizing antioxidant enzymes (peroxidase, catalase, superoxide) and nonenzymatic antioxidants (glutathione, ascorbate, and α-tocopherol). In another context, certain rhizospheric fungal communities can also negatively influence plant productivity by causing disease, for example, Fusarium species, Verticillium spp., and Macrophomina spp., which affects many crops (Tetali et al. 2015). Most studies have focused on rhizospheric bacterial communities. However, very less information is known about the interaction of fungal communities in the plant rhizosphere. Recently developed molecular techniques, metagenomics, transcriptomics, proteomics, and next-generation sequencing studies showed colonization of plant roots by fungal communities that establish information about the changes in expression of plant genes in response to stress, biomolecule synthesis, photorespiration, photosynthesis, and carbohydrate metabolism.

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4.2.2 The Phyllosphere Fungal Microbiome Communities The phyllosphere microbiome is associated with a diverse group of microorganisms, such as viruses, bacteria, algae, yeasts, filamentous fungi, protozoa, and nematodes (Lindow and Brandl 2003; Porras-Alfaro and Bayman 2011). Bacteria are the most dominant and abundant microorganisms in the phyllosphere community (Lindow and Brandl 2003; Vorholt 2012), while fungi are comparatively less abundant. The structure of phyllospheric communities is governed by immigration, survival, growth of the microbial colony, and leaf physicochemical properties (Gomes et al. 2018; Yao et al. 2019). The phyllosphere niche has a high significance in sustainable agriculture and an environmental process that provides confirmation for interactions of phyllospheric microbial communities that affect the health of the natural plant and the quality and productivity of agricultural crops (Boddy et  al. 2008). Filamentous fungi largely occurring as dormant spores in phyllospheric fungal communities rather than active mycelia and population size range between 102 and 108 colony-forming unit/gram of leaf (Andrews and Harris 2000; de Jager et al. 2001). The most abundant fungal communities found on leaves are considered Cladosporium, Alternaria, Penicillium, Acremonium, Mucor, and Aspergillus (Inácio et al. 2002; Porras-Alfaro and Bayman 2011). Filamentous fungi appear to occur ubiquitously as endophytes, and their diversity is particularly observed in long-lived tropical leaves. Fungal endophytes are the second most abundant phyllospheric fungal communities that protect against pathogens and increase abiotic tolerance (Arnold et al. 2000, 2003; Schweitzer et al. 2006). The diversity of cultured yeasts appears as the genera Cryptococcus, Sporobolomyces, and Rhodotorula, either singly or with multiple species in the phyllosphere (Inácio et  al. 2002; Glushakova and Chernov 2004). To explore the phyllospheric fungal species, culture-dependent approaches are applied over 340 genetically distinct taxa of two tropical forests, but still, culture-independent approaches have not yet been reported to characterize fungal diversity.

4.2.3 Endosphere Fungal Microbiome Communities Although less than 100,000 fungal species have been described as an indispensable role of endophytes encompasses a large, hidden component of fungal biodiversity (Arnold 2007; Rodriguez et al. 2009), the dominating classes of fungal endophyte communities included Sordariomycetes, Dothideomycetes, Eurotiomycetes, Leotiomycetes, and Pezizomycetes (Jumpponen and Jones 2009; Atugala and Deshappriya 2015) which are associated with grasses and many woody plant tissues and roots (Alberton et  al. 2010; Bhagobaty and Joshi 2012). Endophytic fungal communities are important components of plant microbiomes that live within plant tissues without causing disease symptoms. Fungal endophytes reside symbiotically

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inside the plant tissue or interact with other microbial groups that colonize in the plant tissues, e.g., mycorrhizal fungi, pathogens, epiphytes, and saprotrophs (Porras-­ Alfaro and Bayman 2011). Some fungal endophytes play an important role in plant growth, resistance to abiotic and biotic stresses, and disease in the plant by producing useful, antagonistic, and signaling molecules (Gao et al. 2010; Khan et al. 2011; Gautam et  al. 2013). Endophytes have a significant effect on the plant fitness, growth, and development by modulating different pathways of plant-like phytohormone (Khan et al. 2012, 2015), antimicrobial compound (Prabukumar et al. 2015), and secondary metabolites (brefelcin A, mevinolin, 2-(3,4-dihydroxyphenyl) ethanol, cytochalasins, polyketides, terpenoids, flavonoids, and steroids) producing pathway (Guo et al. 2008; Balbi and Devoto 2008; Aramsirirujiwet et al. 2016). Because most of the important root endophytes are not culturable, that’s why molecular techniques have been important for identification (Roe et al. 2010;) and confirmed that many of these endophytes coexist with other functional groups in the microbiome. Rapid advances in DNA and RNA sequencing technologies and comparative genomics, transcriptomics, and proteomics approach now facilitate us to study fungal communities in an integrative way, including exploring the taxonomic and phylogenetic profiles of fungal communities in the rhizosphere. In this sequence, their functional and ecological attributes put forward an open discussion about the role of fungal endophytes in the plant microbiome composition, structure, and their diversity, important for plant growth and survival and interactions with another plant-associated microbiome.

4.3

 anipulation of the Plant Microbiome Toward M Improved Plant Health

The rhizosphere, phyllosphere, and endosphere microorganisms both directly and indirectly influence the composition, structure, diversity, and productivity of natural plant communities (Mendes et al. 2018). Microbial species richness provides information about the plant diversity and productivity (Sharma et al. 2015). On purpose manipulation of the plant microbiome may be an alternative way to advance the agriculture sustainability (Bai et  al. 2015). This would be done by manipulating rhizosphere, phyllosphere, and endosphere microorganisms with useful traits. The recent advancement in rhizosphere engineering, manipulation of the rhizospheric microbiome, can aid in the management of soil health and ecological stability (Broberg et al. 2018). The diversity of microorganisms in the soil is increased through crop rotation that promotes high flexibility to plant pathogens (Hwang et al. 2009). The application of certain microorganisms or the introduction of inoculants is one of the emerging strategies for plant microbiome manipulation, and through this approach, a beneficial community effectively replaces the plant pathogenic microbes. The co-inoculation of several beneficial strains, including endophytes, reduces the time of niche (Compant et al. 2010).

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Manipulation of the phyllosphere microbiome can provide a new strategy for enhancing plant growth and health. Falk et al. (1995) suggested that the severity of powdery mildew infections caused by Uncinula necator on grapevines was reduced by releasing the conidia of the mycoparasite fungus Ampelomyces quisqualis. The literature describes several success stories of the use of Trichoderma spp. in mycobiome engineering for biotic stress management (Błaszczyk et al. 2014) and to combat with abiotic stresses by multiple beneficial effects on plant growth and stress tolerance (Singh and Sharma 2012; Chepsergon et al. 2014). Perazzolli et al. (2014) showed that the naturally occurring microbiomes of grapevine leaves could reduce signs of powdery mildew on controlled conditions. A number of reports indicated that growth-promoting and stress-managing fungal communities are applied in rhizosphere, as in the form of liquid and solid formulations to produce active and viable conidia of fungal strains, which are comparatively more tolerant to adverse conditions and provide crop growth in terms of root expansion and nutrient uptake (Waghunde et al. 2016).

4.4

Modern Molecular Tools to Study Plant Mycobiome

The traditional techniques used to identify plant mycobiome relied upon cultural and morphological based approaches. These methods are often time-consuming, laborious, and species-dependent, require extensive knowledge of classical taxonomy, and have the inability to accurately quantify the pathogen (Goud and Termorshuizen 2003). For this reason, the availability of fast, sensitive, and accurate methods is required for detection and identification purpose. These limitations have led to the development of different molecular approaches with improved accuracy and reliability. A variety of molecular methods have been used to detect, identify, and quantify plant pathogenic fungi. Here, we discuss the modern molecular tools and technique to study plant mycobiome, their applicability, and their implementation (Table 4.1). Still, most of the studies on plant mycobiome are based on a culturable technique that involved first isolation of organisms into pure culture and then identification of them, but majority of uncultivable organism is overlooked due to their not or slow-­ growing properties in cultural media. To overcome this constraint, several techniques were developed, viz., direct amplification of DNA from the surface-sterilized plant material and identification of fungal species, multilocus barcode approaches, and next-generation sequencing studies that investigated fungal communities and overall fungal diversity in plant mycobiome. To fingerprint, the most dominant fungal species at different taxonomic levels usually applied denaturing gradient gel electrophoresis (DGGE) or single-strand conformation polymorphism (SSCP). Quantifying fungal biomass in plant tissues can be achieved by real-time PCR techniques that greatly depend on the type of fungus as well as cell size, number, and type and require extensive calibration for each species using pure cultures (Tellenbach et  al. 2010). Next-generation sequencing technologies and systems biology allow simultaneous extension and examination of all members of microbial

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Table 4.1  Different molecular tools used in plant mycobiome study Plant mycobiome organisms Sclerotium rolfsii, Colletotrichum capsici

Purpose of the study Diversity analysis by using ITS region

Cooperational-PCR (Co-PCR)

Grapevine fungi

PCR-DGGE

Phytophthora species

Real-time PCR

Colletotrichum acutatum, Fusarium oxysporum f. sp. ciceris, Discula destructiva, F. poae, Pythium vexans

Sensitive and specific detection of microorganism Detection of multiple species Quantification of a minimal amount of pathogenic microorganisms

Restriction fragment length polymorphism (RFLP)

Pythium myriotylum

Nested-PCR

Numerous fungi

Multiplex PCR

Podosphaera xanthii, Golovinomyces cichoracearum, and Phytophthora lateralis Mycosphaerella graminicola, Oidiumneo lycopersici Blumeria graminis

Method Conventional PCR

Reverse transcription (RT)-PCR In situ PCR PCR-ELISA

Magnetic capture hybridization (MCH) PCR Isothermal amplification methods

Didymella bryoniae, Phoma species, Phytophthora, and Pythium Nectria galligena

Fusarium graminearum, Phytophthora ramorum, and P. kernoviae

Differentiation of pathogenic and nonpathogenic strains Used for detection and/or characterization Detection and differentiation

Detection of viable populations

References Torres-Calzada et al. (2011) and Jeeva et al. (2010) Martos et al. (2011)

Rytkönen et al. (2011) Samuelian et al. (2011), Jiménez-­ Fernández et al. (2011), Zhang, N. et al. (2011), Kulik et al. (2011), and Tewoldemedhin et al. (2011) Gómez-Alpizar et al. (2011)

Hong et al. (2010); Aroca and Raposo (2007), and Grote et al. (2002) Guglielmo et al. (2007) and Chen et al. (2008)

Identification and diversity analysis Detection and differentiation at species level

Guo et al. (2005) and Matsuda et al. (2005) Bindslev et al. (2002) Somai et al. (2002) and Bailey et al. (2002)

Detection at species level

Langrell and Barbara (2001)

Rapid detection and diversity analysis

Abd-Elsalam et al. (2011) and Tomlinson et al. (2007, 2010) (continued)

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Table 4.1 (continued) Method Random amplified polymorphic DNA (RAPD)

Amplified fragment length polymorphism(AFLP)

Microsatellites

DNA arrays

Micro RNA (miRNAs) Induced mutagenesis

Plant mycobiome organisms Fusarium spp. and Elsinoë spp.

Purpose of the study Genetic diversity analysis

Cladosporium fulvum, Pyrenopeziza brassicae, Aspergillus carbonarius, A. ochraceus, Colletotrichum gossypii, C. Gossypii var. Cephalosporioides Ascochyta rabiei, Ceratocystis fimbriata, Macrophomina phaseolina, Puccinia graminis, P. triticina, Sclerotinia subarctica, S. sclerotiorum, and Magnaporthe grisea Fusarium species and Penicillium species

Differentiate fungal isolates at several taxonomic levels

Fusarium head blight (FHB) on wheat Phytophthora nicotianae

DNA barcoding.

Fusarium proliferatum

Transcriptome analysis

Phytophthora capsici, P. infestans

Genetic diversity of plant pathogenic fungi within species and genetic map construction

Differentiation of toxin-producing and nonproducing species. Cox I high-density oligonucleotide microarray identification Genomic study of wheat Identification of Phytophthora blight-resistant mutants Identification at the species level To assess the change in mRNA levels for selected genes and pathogenic variability

References Arici and Koc (2010), Lievens et al. (2007); Hyun et al. (2009), and Hiremani and Dubey (2019) Schmidt et al. (2004) and Silvar et al. (2005)

Jana et al. (2005), Bayraktar et al. (2007), Szabo (2007), Szabo and Kolmer (2007), Winton et al. (2007), and Zheng et al. (2008) Nicolaisen et al. (2005) and Chen et al. (2009)

Kharbikar et al. (2019) Kumari et al. (2019)

Nayyar et al. (2018) Kandel (2014) and Muthuswamy et al. (2018)

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communities and their interactions by using “omics approaches” (metagenomics, transcriptomics, proteomics, and metabolomics). The discovery of emerging molecular technology helps to gather the information about the uncultivable fungal species, but nutritional modes and ecological associations of that fungal taxa are still challenging for the researchers (Tedersoo and Nilsson 2016). As DNA sequencing technologies progressed from sequencing single specimens to parallel Sanger sequencing in the early 2000s, it brought inspiration to researchers to reveal the unseen mycobiota and their diversity, structure, functioning, and significance. Sanger and Maxam-Gilbert sequencing technologies were considered as first-generation (the 1990s), most common sequencing technologies used by researchers because of its high efficiency and low radioactivity until the emergence of a new era of sequencing technologies opening new perspectives for genome exploration and analysis (Pareek et  al. 2011). The second-­ generation sequencing methods were developed in the 2000s and marked the beginning of high-throughput sequencing (HTS) which were characterized by the need to prepare amplified sequencing banks before starting the sequencing of amplified DNA clones to analyzed the hidden fungal communities (Vezzi 2012; Qiang-­long et al. 2014). The second-generation sequencing included pyrosequencing, Illumina sequencing, Ion Torrent semiconductor sequencing, and SOLiD (Supported Oligonucleotide Ligation and Detection) sequencing (Kchouk et  al. 2017). NGS technologies continue to improve, and the number of sequencers increases these last years. However, the third-generation sequencing performs at the level of single molecules and produce higher read lengths than the earlier generations that overcome the problem of the necessity to create the amplification libraries. Also, third-­generation sequencing can produce long reads of several kilobases for the resolution of the assembly problem and repetitive regions of complex genomes which is useful in metabarcoding and community analysis of mycobiome (Song et al. 2015; Rhoads and Au 2015; Nilsson et al. 2018). This chapter briefly discusses the application of different HTS, which elucidate the study of fungal community associations related to taxonomic profiling of fungal communities and their mycobiome structure, function, signaling mechanism, and ecosystem functioning.

4.5

Major Applications of Plant Mycobiome

Recently, plant-associated fungal communities have been taken a greater interest as bioinoculant to enhance plant growth in different kinds of biotic and abiotic stresses. Thus the rhizospheric engineering involves the development of new strategies to reshape the rhizospheric microbiome for biofertilization and induces root growth stimulation, antibiosis, induced plant systemic resistance, and parasitism. These microorganisms follow several mechanisms to support plant growth which include the production of phytohormones and the mobilization of organic matter and minerals, like carbon, nitrogen, phosphorus, and iron (Tkacz and Poole 2015). The mechanisms of suppression of pathogens demonstrate several direct

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interactions with plant pathogens, as well as indirect interaction, which include stimulation of the plant immune system or systemic resistance (Lugtenberg and Kamilova 2009).

4.5.1 Plant Growth Promotion Plant-associated fungal community structure and metabolism are altered during development and environmental changes, as the nutrients are provided in the microbiome by the plants. So in these consequences, secretion of the nutrients exuded by different plants, the specific fungal pathways responding to them, and the mechanisms by which plant-associated fungal community activates or repress the root colonization process in the response of exudate (Contreras-Cornejo et  al. 2016; Zeilinger et  al. 2016). Fungal community interactions in plant microbiota likely play determinative roles in colonization of the host plant, plant growth promotion, nutrient uptake, microbiome succession over plant development, and the ability of mutualists to suppress pathogen growth (López-Bucio et al. 2015; Guler et al. 2016; You et al. 2016). Several researchers reported Trichoderma colonized plants to secrete different bioactive compounds like auxins, ethylene, gibberellins, plant enzymes, antioxidants, etc. for signaling molecule between mycobiome and compounds like phytoalexins and phenols that provide tolerance to abiotic stresses and enhance the branching capacity of the root system (Brotman et al. 2013; López-­Bucio et al. 2015). Application of plant growth-promoting fungi Trichoderma longibrachiatum T6 enhances the tolerance of wheat to salt stress through the improvement of the antioxidative defense system and gene expression (Zhang et al. 2016). The plant microbiota also influences the composition of plant secondary metabolites and the resulting development of different metabolites. Studies on the influence of the microbiome on the taste of strawberries (Zabetakis et al. 1999; Verginer et al. 2010) and the production of metabolites in medicinal plants (Köberl et al. 2013; Schmidt et al. 2014) have been reported. In a study on Arabidopsis thaliana, the rhizosphere microbiome could be linked to insect feeding behavior, which was most probably a result of microbiome-driven changes in the leaf metabolome (Badri et  al. 2013). Peñuelas et al. (2014) showed that the removal of the floral microbiome of Sambucus nigra resulted in a reduced floral terpene emission, which plays an important role in pollination and consequently in fruit and seed production.

4.5.2 Disease Management The plant microbiome is effectively involved in pathogen suppression, particularly the plant mycobiome that acts as a protective armor against phytopathogens (Weller et al. 2002). The various mechanisms are involved in direct interactions with phytopathogens as well as indirect interactions via mechanisms of parasitism, competition for nutrients, and induction of systemic resistance against abiotic and biotic stresses (Lugtenberg and Kamilova 2009). The recent research has shown that the

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plant mycobiome is involved not only in managing with biotic stress but also in protection against abiotic stress (Bragina et al. 2013). Several reports indicated that Trichoderma spp. have beneficial effects on plant growth and biotic stress management in different horticulture crops like radish, cucumber, pepper, bottle gourd, periwinkle, bitter gourd, chrysanthemum, lettuce, and tomato (Donoso et al. 2008; Bae et al. 2009; Brotman et al. 2013; Contreras-Cornejo et al. 2016; Zeilinger et al. 2016). Kotasthane et al. (2015) reported the antagonistic potential of Trichoderma spp. against Sclerotium rolfsii and Rhizoctonia solani and their plant growth promotion response toward the growth of cucumber, bottle gourd, and bitter gourd. The ongoing research is an effort to elucidate the molecular basis of plant mycobiome to gather broad perspectives regarding their functioning and applicability for growth promotion and defense activation of the plant in disease management (Table 4.2).

4.6

Conclusion and Future Prospects

This review was undertaken to explore the current information on plant mycobiome management and focused on developing technologies to overcome the constraints related to mycobiome engineering. Recent advancement in molecular technologies and ongoing research have revealed the greater diversity and complexity of plant mycobiome rather than previously imagined, while an amalgamation of biochemical, molecular, and genetic approaches has led to new visions into the exact mechanism of signal induction and transduction processes of secondary metabolites from fungal communities in plants and other organisms. The ongoing research, technological advancement in molecular biology, and high-throughput omics included genomics, transcriptomics, proteomics, and metabolomics that provide information to elucidate the role of the mycobiome gene that aids in improving plant performance. Therefore, the better understanding of metagenomics, genetic sequence information of microbiome, obtained from next-generation sequencing data has substantial potential for the discovery of diversity and functional perspective of the sequenced genes of the microbiome-related organisms. Looking forward toward the potential of NGS data to demonstrate the functional diversity of mycobiome will require an elucidation of basic biology of fungi through traditional culturing approaches and sequencing of individual fungal genomes to demonstrate the evolutionary studies in natural habitat. Here, this chapter reviews omics-based approaches that are driving forward the current understanding of plant-associated fungal gene functions and describes how these technologies have helped unravel key bacterial genes and pathways that mediate pathogenic, beneficial, and commensal host interactions.

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Table 4.2  Beneficial and pathogenic mycobiome association with different crops Antagonist Trichoderma hamatum and T. harzianum Glomus sp. and Trichoderma sp.

Pathogen Fusarium oxysporum f. sp. cepae Cryphonectria parasitica

T. viride

Macrophomina phaseolina

Trichoderma spp., T. brevicompactum, T. gamsii, and T. harzianum Piriformospora indica

F. oxysporum, Pythium spp., and Rhizoctonia solani (Kuhn.)

Trichoderma harzianum strain Th22 T. harzianum,

T. viride and Ampelomyces quisqualis

Fusarium spp.

F. graminearum

M. phaseolina, Fusarium oxysporum f. sp. cumini Oidium euonymi-japonici

T. viride isolate NRCL T-01

F. solani

T. harzianum

M. phaseolina (Tassi) Goid

Counter mechanism Induction of antifungal compounds Induction of secondary metabolites Antagonist mechanism by mycelial destruction Production of the enzymatic machinery

Induction of antimicrobial product, enzymatic mechanisms, and plant growth promotion Activation of defense-related genes Induction of secondary metabolites Antagonistic mechanism by mycelial destruction and mycolytic enzyme production Mycolytic enzyme production Induction of secondary metabolites

Host plant Onion

References Adèle et al. (2019)

Chestnut

Murolo et al. (2019)

Mung bean

Shahid and Khan (2019)

Tomato

Biam et al. (2019) and Bader et al. (2019)

Sugarcane, potato, peas, maize, soybean

Aslam et al. (2019)

Maize

Saravanakumar et al. (2018)

Guar, moth bean, mung bean, and sesame Euonymus japonicus

Mawar et al. (2019)

Ahanger et al. (2018)

Litchi

Kumar et al. (2018)

Mungbean

Thombre and Kohire (2018) (continued)

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Table 4.2 (continued) Antagonist Massarina igniaria, Periconia macrospinosa, Noosia bankssiae, Flavomyces fulophazii Acremonium, Arthrinium, Botryotinia, Chaetomium, Dictyosporium, Humicola, Ilyonectria, Mucor, Myrothecium, Penicillium, Periconia, Thielavia T. harzianum

Pathogen –

Host plant Oryza sativa

References Vergara et al. (2018)

Alternaria panax, Fusarium oxysporum, Fusarium solani, Phoma herbarum, and Mycocentrospora acerina

Induction of antimicrobial product, enzymatic mechanisms, and plant growth promotion

Panax notoginseng

Zheng et al. (2017) and Nandhini et al. (2018)

F. graminearum

Antagonistic activity by mycelial destruction and nutrient competition Induction of antimicrobial product, enzymatic mechanisms, and plant growth promotion Interaction and mycolytic enzyme production Plant growth promotion and phytohormone production Antagonistic and biocontrol potential Mycoparasitism and mycolytic enzyme production

Maize

Saravanakumar et al. (2018)

Teucrium polium

Hassan (2017)

Gladiolus

Khan et al. (2017)

Parthenium hysterophorus

Priyadharsini and Muthukumar (2017) Li et al. (2016)

Penicillium chrysogenum and P. crustosum

Staphylococcus aureus, Salmonella typhimurium, and Candida albicans

T. harzianum

F. oxysporum f. sp. gladioli and Meloidogyne incognita –

Curvularia geniculata

Counter mechanism Plant growth promotion and phytohormone production

T. asperellum ZJSX5003

F. graminearum

T. harzianum, T. viride, A. flavus, A. falcatum, and A. niger

Colletotrichum falcatum

Maize

Sugarcane

Suresh and Nelson (2016)

(continued)

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Table 4.2 (continued) Antagonist T. viride A. niger and T. harzianum

Pathogen Pestalotia theae and F. solani. Fusarium spp., R. solani and M. phaseolina

Trichoderma isolates

F. fujikuroi

Trichoderma isolates (TvO, TvG, ThC, ThR, and ThM)

R. solani, Sclerotium rolfsii, M. phaseolina, F. oxysporum, A. niger Macrophomina spp.

Trichoderma viride Trichoderma spp.

Lasiodiplodia theobromae

Glomus mosseae, T. harzianum, and P. simplicissimum

Rhizoctonia solani

Counter mechanism Hyphal swelling and distortion Mycoparasitism and mycolytic enzyme production Antibiosis and biocontrol potential Induction of secondary metabolites

Antagonistic and hyphal swelling and distortion Induction of secondary metabolites Induction of antimicrobial product, enzymatic mechanisms, and plant growth promotion

Host plant Tea Cowpea and mungbean

Rice

Okra, maize cauliflower, and groundnut

References Naglot et al. (2015) Ikram and Dawar (2014)

Bhramaramba and Nagamani (2013) Pan et al. (2013) and Gajera et al. (2011)

Jute

Srivastava et al. (2010)

Elaeocarpus munronii

Priya and Nagaveni (2009) Chandaniea et al. (2009)

Cucumis sativus

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5

Role of Soil Fauna: En Route to Ecosystem Services and Its Effect on Soil Health Apurva Mishra and Dharmesh Singh

Abstract

Soils have an amazingly assorted network of soil fauna that contrast in their versatile procedures, and consequently, in the capacities, they satisfy in soils. Soil fauna works as an extremely proficient means, which aids microorganisms in inhabiting and broadening their venture furthermore into the soil skylines. Lives of soil fauna as soil settlers, indicators, and architects have been underlined, but recent research and worldwide natural concerns are urging the scientific community to look further into the controls of soil fauna for sustainable management of soils in these turbulent times. Molecular data alone is insufficient for many investigations about soil fauna, and hence there is a need for sincere efforts in increasing expertise in the classical taxonomy of soil fauna. This specialization, along with data on the soil fauna’s biogeography, their relationship to over-the-­ ground problem areas, and land management schemes, will be acute for accepting how soil fauna will communicate and react to numerous worldwide alterations. This chapter discusses the soil fauna on the soil grounds as well as below grounds, tight associations of abiotic factors with the soil biodiversity, their roles in ecosystem events and functions, and, finally, the arrangement of ecosystem benefits for human prosperity. A proper and researched thought about soil faunal species, their identities, geographic extents, and an understanding of their roles in soil and land management will help in giving balanced forecasts for the working of future biological communities that are under siege due to inevitable environmental climate change. A. Mishra Academy of Scientific and Innovative Research (AcSIR), Ghaziabad, India Environmental Biotechnology and Genomics Division, CSIR-National Environmental Engineering Research Institute, Nagpur, Maharashtra, India D. Singh (*) Environmental Biotechnology and Genomics Division, CSIR-National Environmental Engineering Research Institute, Nagpur, Maharashtra, India © Springer Nature Singapore Pte Ltd. 2020 M. K. Solanki et al. (eds.), Phytobiomes: Current Insights and Future Vistas, https://doi.org/10.1007/978-981-15-3151-4_5

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Keywords

Soil fauna · Soil biodiversity · Soil health · Ecosystem engineers · Faunal indicators

5.1

Introduction

Soil speaks as a standout among the essential supplies of biodiversity. It reflects the environmental metabolism since all the biogeochemical procedures of distinctive biological systems are consolidated inside it. It is an intricate framework comprising biotic and abiotic segments, which coordinates with the essential habitat and ensures biological activity and diversity, assisting ecosystem services (Robinson et al. 2013). Inside the composite assembly of soil, biotic and abiotic parts communicate in governing the natural debasement of materials and nutrient cycling (Morgado et al. 2018). Soil fauna or the biotic portion of the soil is an imperative store of biodiversity and assumes a basic role in several soil biological system capacities. Soil environmental conditions are degrading due to the increase in human activities, leading to a reduction in the abundance of plants and animal communities responsible for a balanced environment (Morgado et al. 2018). The consequence of this biodiversity loss is a counterfeit environment that needs steady human intervention and requires additional expenses, while regular ecosystems are optimally controlled by a group of plants and animals and a thorough supply of energy and nutrients—a form of control gradually vanishing with land-use change and industrial growth. As a result, agricultural practices that permit a mix of production targets and ecologically amicable administrations work sustainably, ensuring healthy soil biodiversity, which is fundamental to preventing soil fauna networks from declining in agricultural lands and also helping us in understanding their role toward ecosystem services.

5.2

Structure of Soil Ecosystem

5.2.1 Soil Organization Amid biological communities, soil stands as the focal organization, incorporating a huge number of geochemical and ecological capacities (Coleman and Whitman 2005; Crawford et al. 2005; Wall et al. 2010, Delgado-Baquerizo et al. 2019). Soils’ position exists at the interface media (Fig. 5.1), located at the intersection of the four main life-supporting provinces: lithosphere, hydrosphere, atmosphere, and the biosphere (living matter). This provides exceptionally dynamic and multiphasic character to the soil, where numerous estimated aggregates are connected and balanced out inside a perplexing lattice of solid, fluid, and gaseous parts communicating at different scales (Lal 2016; Parker 2010).

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Fig. 5.1  Pedosphere presenting biotic and abiotic interactions in the soil matrix (Modified from Fitzpatrick [1984] and Coleman and Crossley [1996])

Soil particles do not make a nonstop and conservative mass; instead, the soil volume is framed by pores, chambers, channels, and splits that give an appropriate domain to soil fauna and lead to the development of plant roots. This physical organization in soil additionally directs the motion of gases and fluids inside the soil making different land- or water-capable situations, heterogeneously loaded up with soil “solution” and mostly occupied with gases, which are critical for the soil fauna (Lavelle 2012). A wide variety of dissolved and suspended matter, including inorganic and organic materials, contributes toward soil “solution” composition (Lavelle and Spain 2001). Soil components engaged on the solid stage diffuse to the fluid stage. In this manner, minerals and organic matter end up being accessible to the larger part of soil-living creatures and plants. Soil gaseous stage permits oxygen (O2) utilization and carbon dioxide (CO2) generation amid biological exercises. As the soil O2 gets used up, usually there is a trade-off between the soil and atmospheric O2 with the help of a concentration gradient, with CO2 transition happening in reverse. Relative humidity of terrestrial ecosystems remains near saturation, which is indispensable to most soil fauna, for instance, in the case of springtails. Nematodes, on the other hand, can survive at different levels of relative humidity (Lavelle and Spain 2001) Notwithstanding the huge predisposition toward the above-ground portion of the soil ecosystem, it is the below ground, the subterranean, where indispensable biodiversity focused on the pore spaces resides (Beare et al. 1995). Pore spaces have an expanded surface territory that makes a large number of active microenvironments

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where neighborhood species are exposed to low, competitive exclusion, and concurrence is set between these neighborhood species through resource partitioning (Haynes 2014; Lavelle 1997). For instance, low water potential causes low pore connectivity, hence responsible for the increase in the bacterial abundance (Carson et al. 2010). Competition acts as organizing power for biota consensus in the soil, limited to finer scales, for instance, soil aggregates for microbial networks or the soil pore space and rhizospheric area for microfauna, where prospective contenders may utilize a similar space and accessible resources (MEA 2005).

5.2.2 Soil Biodiversity On earth, soils are the most phylotype-rich environments (Giller 1996). No place in nature is plausible enough to discover such a large number of organisms as in soil ecosystems (Hågvar 1998). Unfortunately, despite the immense efforts by scientists in the past few years to portray and comprehend soil networks, the taxonomic shortage for soil biodiversity is the biggest mysteries (Decaëns 2010) and little is known about the soil’s cryptic biodiversity (Bardgett and van der Putten 2014). In spite of this fact, one perspective as of now remains undisputable: soil biodiversity is obligatory for an optimum level of soil functioning that eventually supports all soil-based ecosystems and goods (Barrios 2007). Subsequently, enriching the information about soil biodiversity is foremost to completely comprehend the fundamentals of soil health, adequately oversee soil-based environmental benefits, and foresee future patterns and situations for the recent period (Bardgett and van der Putten 2014). Soil organisms are hyperdiverse and amazingly unpredictable and incorporate soil communities from all major scientific categorizations (Parker 2010; Wardle 2006). They are typically arranged depending on their body size, whose variety inside soil networks traverses a few orders of size (Barrios 2007; Lavelle 2012; Parker 2010). A greater part of decent soil variety is created by microbiota or microscopic organisms such as bacteria, archaea, and fungi; however, it includes an exceptional range of microfauna, mesofauna, macrofauna, and even megafauna (Bardgett 2002; Lavelle 2012; Orgiazzi et  al. 2016; Wurst et  al. 2012). Also, it incorporates a tremendous assortment of photosynthetic entities like lichens, bryophytes, and vascular plants, and their root systems have significant roles in soil ecosystem organization (Orgiazzi et al. 2016). Soil microbiota contributes, for the most part, to decay forms, favoring carbon (C), nitrogen (N2), and other biogeochemical cycling, yet also assume a vital role in defeating disease and in plant growth and development (Wurst et al. 2012). These life forms make vital cooperative collaborations with plants, such as enhancing nutrient uptake (e.g., N2 fixation, phosphorus redistribution), as well as manage plant hormones (Wurst et al. 2012). Soil organic matter (SOM) is critical for the biological processes and supply of nutrients, in every variety of soils. Two to ten percent of the soil mass is SOM, which is essential for the comprehended function, including physical, chemical, and biological functions. SOM has been instigated in plants, which can be categorized into “living” and “dead” components during different stages of decomposition and

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varies in age from fresh residues to those that are years old in the form of resistant organic matter. Carbon and other organic particles, such as hydrogen (H2), oxygen (O2), and little amounts of N2, phosphorous, sulfur, potassium, calcium (Ca), and magnesium (Mg), constitute SOM. Nearly 5–10% of below-ground SOM contains roots, fauna, and microorganism, that is, living, and this living pool of microbial components is referred to as microbial biomass, which is considered essential for decomposition of organic matter, nutrient cycling, chemical degradation, and stabilization of soil (Ha et  al. 2008). During early plant development, phosphorus is required for cell growth. Soil phosphorous can be distributed into three pools, each varying in its accessibility to plants: 1 . Soil organic phosphorus bound to organic compounds 2. Inorganic compounds (phosphorus joined with Ca, Mg, iron (Fe), aluminum (Al), or clay minerals) 3. Natural and inorganic phosphorus compounds related to living cells Soil phosphorus moves between each of these pools using mineralization (separate of natural matter), immobilization, and redistribution of phosphorus between microorganisms, plants, and natural matter. Phosphorus is immobilized (made inaccessible to plants) when it is consolidated into the living microbial biomass. Redistribution of phosphorus happens when phosphorus is discharged from microbial cells and moved into different phosphorus pools. Phosphorus mineralization and immobilization happen at the same time in soil. While mineralization of natural soil phosphorus to inorganic phosphorus expands the accessibility of phosphorus to plants and microorganisms, an extensive amount (between 15 and 80%) of soil phosphorus stays in natural structure and remains inaccessible to plants (Ha et al. 2008). Soil microfauna incorporates organisms that are ≤100 μm (e.g., nematodes, protozoa, and rotifers) in size. Only one taxon, protozoa, is discovered completely inside this class (Ruggiero et al. 2015). Mainly, mites, nematodes, rotifers, tardigrades, and copepod scavengers fall inside this group (Kennedy and Gewin 1997). Soil microfauna feeds on microscopic organisms such as fungi and algae, yet they additionally represent predator and saprophytic gatherings too. Through their actions they manage: (1) nutrient cycling by enhancing the accessibility of nutrients to different species (e.g., excretion), (2) population and actions of microscopic organisms and fungi, and (3) scattering of pivotal rhizospheric microbiota (Wurst et  al. 2012). Their impacts on plants are likewise—when in direct contact with roots, they benefit from the root excretions and modify the plant’s defenses or hormones. The role of plant roots in soil processes cannot be separated from the varied group of organisms, which flourish around them. These comprise parasites too, herbivores and predators, nematodes or worms as microbial grazers, and free-living microbes feeding on root exudates. Secondary metabolites produced by plants such as iridoid glycosides are present in root exudates. Other volatile organic compounds (VOCs) are also released by green leaves and above-ground roots that attract pollinators. Below-ground roots also release VOCs that dissuade soil-inhabiting herbivores.

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Likewise, plants are not just providers of litter for decomposers but rather they assume a functional job in pulling in valuable soil invertebrates. For instance, plants draw in entomopathogenic nematodes to kill the rhizospheric herbivores, giving innoculum to the rhizospheric bacterial population, aggravating the correspondence between destructive microorganisms, and furthermore, in adjusting rhizodeposition and root architecture. This eventually results in a better communication between soil fauna and plant roots (Briones 2018). All these synthetic signs discharged by the plants are coordinated in a way that profits their very own development and health. Soil mesofauna ranges from 100 μm to 2 mm (gatherings include taxa like Acari, Collembola, Tardigrada, Protura, Diplura, and Enchytraeidae) in size. Microarthropods, for example, mites and springtails, are the fundamental organisms of this group. They could be classified into herbivores, bacterivores, or fungivores. At times, they can additionally gorge on higher trophic dimension life forms. They live near the air and water existing in soil and are thus exceptionally reliant on soil aeration and humidity. Soil mesofauna helps in nutrient cycling and management of pests and disease control by their preferential mode of feeding, acts as food for other soil organisms, and aids in soil fauna distribution (Wurst et al. 2012). Soil macrofauna (>2 mm in size) is fundamentally in charge of litter comminution and redistribution, and predation on other soil-abiding organisms frequently called as “ecosystem engineers.” Macroarthropods (e.g., isopods, spiders, bugs) alongside annelids and gastropods are the fundamental congregations of soil macrofauna. These creatures are in charge of modifying the structure of their natural surrounding by contributing to various soil capacities, like physical disintegration and transport of litter residues to lower layers of soil that eventually help in nutrient cycling by microfauna and microbes, water penetration (e.g., by burrowing practices), and pest and disease control (rich biodiversity and predation; Wurst et  al. 2012). They have an immediate constructive outcome on plant development and yield, yet they could be the reason for some harmful impacts on crops. Soil megafauna (soil fauna whose size surpasses 20 mm): Individuals from this group incorporate an extensive range of invertebrates (worms, snails, myriapods) and vertebrates (insectivores, terrestrial and aquatic rodents, and reptiles). Moles, voles, gophers, snakes, and burrowing owls are few examples of soil megafauna, which help in the breakdown of the complex substances in decomposing plants and animals so that living plants and other organisms can utilize them. This comprises soil organisms as promoters in biogeochemical cycles, with carbon (C) cycle being the most prominent followed by nitrogen (N2) and sulfur (S) cycles. Soil life forms can be characterized additionally as per their usefulness, which makes a difference to explain about their environmental roles in soil systems. Turbé et al. (2010) recommended the utilization of three widely inclusive practical gatherings: chemical engineers, biological regulators, and ecosystem engineers (Fig. 5.2). Creatures directly participating in carbon and other biogeochemical cycles, including nitrogen, phosphorus, and sulfur cycles, and helping in soil decomposition and transformation can be classified as the chemical engineers. Biological regulators are in charge of monitoring the changing aspects of soil inhabitants, thereby advancing the strength and constancy of soil biological systems (Fusaro et al. 2018). Ecosystem

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Fig. 5.2  Classification of soil beneficiaries and their appropriate role in the maintenance of agroecosystem

engineers are in charge of maintaining the soil structure by advancing the formation of stable aggregates (unit of soil structure), the pore network construction, and the advancement of complex biostructures. In spite of a long history of studies focusing on the enumeration of soil fauna (Menta 2012), it is still extremely hard to give precise biomass estimates for soil fauna. This is somewhat due to their inconsistency in time and space (Menta 2012) and also due to contrasts in the methodologies used for their inspection (Wall et al. 2001). Also, most of the studies are from the temperate zones while other climactic/ ecological regions have been genuinely disregarded (Turbé et al. 2010).

5.3

Soil Fauna Organization in the Ecosystem

Soil fauna is viewed as an all-inclusive imperative part necessary for reusing organic matter, soil vitality, and nutrient cycling (Jeffery and Gardi 2010). In conjunction, they are the main players in supporting and managing environment services. Hence, soil biologists frequently organize soil fauna in terms of their broad functions divided into three categories: chemical engineers, biological regulators, and ecosystem engineers (Fig. 5.2). 1. Chemical Engineers: They are the key components of the soil food web. Bacteria and fungi make up the largest portion of this group and also include algae and

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viruses (viruses could impact C cycling through viral shunt where, by bacterial cell lysis, they build up the concentration of labile C in the soil ecosystem that eventually serves toward increment in microbial generation and respiration in soils; refer to Williamson et al. [2017] and Trubl et al. [2018] for more details on this topic). These microscopic engineers help in the decomposition of organic material and transforming complex forms of carbon and nitrogen into CO2 and simpler nutrients (Coleman and Crossley 1996). For their survival and growth, they depend on optimum soil moisture, suitable atmospheric conditions, and pore spaces between soil particles. Significant quantities of organic matter and animal manure in soil environments certify their prevalence. Moreover, they are key parts of a soil food web or sustenance networks as their action ensures the growth of living organisms, commencing from plants to the animals that feed upon them, responsible for organic turnover. Rough evaluations of soil biodiversity demonstrate a few thousand invertebrate species for every site and additionally ambiguous levels of microbial and protozoan variety that contributes in each of the trophic level (Turbé et al. 2010). 2. Biological Regulators: They are the diverse group of soil organisms that control the activities of the subordinate chemical engineers and form a vital link in the food web. Some act as plant pests and parasites, while others stimulate microflora. Their movement around the soil assists fragmentation of organic material, providing more surface area and hence enhancing the availability of the nutrients to microbes. In this group, protists are the smallest organisms, which live in the water layer surrounding soil particles and control bacterial populations through feeding. Nematodes, microarthropods, and protists are the most abundant biological regulators. 3. Ecosystem Engineers: Of major significance in the ecosystem, soil advancement, and support are the alleged “ecosystem engineers,” as these species control, either straightforwardly or in a roundabout way, the accessibility of resources to other co-inhabitants of soil (Davies et al. 2019; Wright et al. 2002). These life forms physically change, keep up, and make new habitat for other life forms. Typically, there are two types of ecosystem engineers—firstly, the allogenic ones that modify the soil background by transforming living or nonliving things from one physical state to another, via mechanical or other means, and, secondly, the autogenic ones that change the soil background using their physical structures, that is, their existing and/or dead tissue (Byers et al. 2006; Lavelle and Spain 2001; Wright et  al. 2002). A precedent of physical “ecosystem engineers” is plant roots that make substantial voids (spaces) in the soil through root rot (Byers et  al. 2006). Termites and earthworms assume a noteworthy role in moving, blending, and circulating air through the soil through their tunneling. Soil fauna is a very important entity, and the greater part is exceedingly versatile, stretching from herbivores to omnivores and even include carnivores. Contingent upon the accessible nutrient supply, a good chunk of soil fauna can modify their feeding systems from a more noteworthy to a lesser degree with instances where numerous carnivorous species amid low food accessibility can head toward the

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transformation and organic matter turnover (Brose and Scheu 2014). The cooperation between soil fauna and ecosystem are various, and unpredictable, due to the huge diversity and prevalent shifts. The level of connection amid soil fauna and the soil itself can vary significantly between taxa and is subjected to soil existence cycle (Wall et al. 2001). Specifically, in conjunction with their physical forms and the ecological roles, it is conceivable to arrange soil fauna into four fundamental gatherings: incidentally dormant geophiles, briefly dynamic geophiles, periodical geophiles, and geobionts (Fig. 5.3). It is noticed that this classification does not have any taxonomical importance, yet, rather, they are helpful after contemplating the existential procedures of soil invertebrates. Incidentally, dormant geophiles are life forms residing in the soil for a certain period of their lifecycle, for example, during hibernation or while experiencing transformation, at a point when security from climatic forces is essential (Menta 2012). Because of their relative dormancy, these life forms affect the natural capacity of the soil, even though they can act as prey for different creatures in this critical

Fig. 5.3  The primary four fundamental gatherings of soil invertebrates contingent upon their life techniques and how nearly they are connected with the soil

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time of their lifecycle. They spend time in the soil to let pass adverse atmospheric conditions, or for metamorphosis; for instance, caterpillars of butterfly families like Noctuidae, Geometridae, or Sphingidae bury themselves in the ground at the time of nymphosis. These incidentally dormant geophiles exert no mechanical force on soil (Menta 2012). Briefly dynamic geophiles reside in the soil in a steady state for an extensive period of their life (i.e., for at least one or more developmental phases and rise out of the earth as an adult). A large portion of these creatures is insects, for example, Neuroptera, Diptera, Coleoptera, and Lepidoptera. Organisms with “pupal” phase in their life cycle assume a minor role in the soil amid this stage, while the “larval” phase is considerably more imperative for the soil ecology, particularly at times where populace thickness is high (Wall et al. 2001, 2008). Most larvae in the soil can go about as both detritivores and predators. Periodical geophiles reside for a significant portion of their life in the dirt, for the most part as hatchlings; however, for the duration of their lives, they at times return to the dirt to perform different exercises, for example, chasing, egg laying, or to flee from threats. A few Coleoptera gatherings (e.g., carabides, scarabeids, cicindelids) pass their larval phase in the litter or the upper layers of mineral soil, and when they reach a mature stage, they utilize soil as a nourishment source, a shelter, and for different purposes (Wall et al. 2001, 2008). Geobionts are living beings that exceptionally spend their entire lifecycle in soil and cannot leave this condition even for a limited period. They have characteristics that counteract survival outside of the soil environment either because they are deficient in ways to secure themselves from desiccation or temperature changes, or are lacking the sensory organs essential to survive above the ground, for example, lacking appendages, necessary for discovering nourishment above ground or for protection from predators. A few types of myriapods, isopods, Acari, mollusks, and the larger part of Collembola, Diplura, and Protura have a place with this gathering (Wall et al. 2001). These distinctive sorts of connections between soil life forms and the soil decide a separated level of weakness among different gatherings and as a result of any conceivable effect on soil condition. In case, if soil pollution happens due to some human interference, geobionts will be the most severely affected group as they cannot leave the dirt and must consume all their time on earth there.

5.3.1 Soil Networks Soil organisms are the principal intermediates of soil working at various scales. The investigation of soil biodiversity began through surveying soil food networks as a feeding web between organisms—one of the major integrating features of soil communities. Natural ecosystems contain numerous species that are associated with their feeding connections over various trophic levels to make a complex food web (Digel et  al. 2014). Consumer and producer interactions can be envisioned as a binding principle for food webs in different ecosystems with hierarchical

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Fig. 5.4  Soil network showing linkages between the different functional groups of soil fauna, along with their role in different soil biological functions

associations acting as a backbone (Brose and Scheu 2014; Digel et al. 2014; Fontaine et al. 2011). Figure 5.4 delineates the various hierarchical associations of the determinants of soil forms (Beare et al. 1995). The arrangement of elements influencing soil working is resolved at both spatial and temporal scales (Wu and Wang 2019). Different organisms, including higher plants and creatures, assume considerable roles in this regard. The working of the soil framework is additionally controlled by: • The deterioration rates of dead organic materials and the equalization between mineralization (which discharges nutrients accessible to plants and microorganisms) and humification (which frames stores of soil organic matter or SOM and colloidal organic mixes) • The level of synchronization of nutrient discharge with plant request • The soil physical structure, which decides the rates and examples of gas trade, soil water movement into and through the soil, and disintegration rates • The texture of the soil (percent of sand, silt, and clay), which impacts the action of soil life forms and henceforth the soil biological working Soil food networks are created by two fundamental frameworks: one, herbivory based (“green” food networks) and the other detritus based (“brown” food networks; Briones 2014). In herbivory-based food networks, plant roots establish the fundamental basal reserve, grazed by plant-feeding nematodes and insects,

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which in turn are grazed by a predaceous network ranging within a few trophic levels (Parker 2010). The brown food network is composed of recalcitrant, nonliving organic materials, supported by the detritus pool. Two vitality channels have been distinguished inside brown food networks: (1) the bacterial vitality channel, with microorganisms as essential decomposers, and (2) the fungal vitality channel, where they are the decomposers (Ramsden and Kervalishvili 2008). This bacterial–fungal vitality channel idea by and large adopts a sensibly well-separated network of detritivores/microbivores (Coleman 1996). Moreover, expanding confirmations recommend that omnivory and feeding versatility is summed up inside soil food networks (Jordán 2009), not only at higher trophic levels but also inside detritivores/microbivores organizations (Gupta and Malik 1996). This entire system, counting the distinctive vitality channels, is balanced out by a broad number of trophic and nontrophic collaborations at different spatial and temporal scales (Ramsden and Kervalishvili 2008). Interactions between networks happen at predator levels (Parker 2010), as well as among autotrophs and decomposers, either connected by uneven metabolic abilities (Giller 1996) or resource competition (Hågvar 1998; Scheu 2002). Nontrophic interactions, for example, the movement of soil engineers, are additionally thought to advance assorted variety and decrease competitive interactions, thus contributing to balance soil food networks (Thompson et al. 2012).

5.3.2 Soil Health and Faunal Indicators Soil health suggests the limit of soil to work as an indispensable living framework, a dynamic framework. It includes the knowledge of soil as a powerful living organism that works comprehensively relying on its condition or state. Soil health relies upon the joined impacts of three noteworthy connecting parts. These are the chemical, physical, and biological attributes of the soil (Cardoso et al. 2013). Soil health is upgraded by the management and land-utilization choices that consider the various functions of soil. It is weakened by choices that look just on single capacities and momentary arrangements, for example, expanding yet not sustaining crop productivity. Soil organisms apply a noteworthy power over many soil forms through their impacts on the deterioration of dead natural material, nutrient cycling, the change and transport of soil materials, and the development and support of soil structure (Griffiths et  al. 2018). Though occasionally not easily perceived, the biological activity of soils is to a great extent gathered in the topsoil, from a couple of centimeters to a depth of 30 cm. The living segment of SOM comprises of: • • • •

Dissolved organic matter made up of soluble root exudates Particulate organic matter, including each of fresh residues and living organisms Humus content Resistant organic matter

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Dead organic matter is at first mostly devoured by macrofauna, comminuting and redistributing it into smaller sections. These partially degraded organic residues are then accessible to meso- and microfauna and microorganisms. Through its tunneling movement, soil macrofauna mixes organic matter profoundly into the soil and stimulates the movement of microorganisms. In this manner, soil organisms take an interest in a variety of procedures fundamental to the working ecosystems. For instance, they assume an imperative role in the cycling of SOM and nutrients in the soil, water purification, agrochemicals detoxification, and in the change of soil structure. Among the capacities directed by soil organisms that help in maintaining the soil health are: • Decay: separating litter, making hummus, and nutrient cycling • Atmospheric N2 conversion into organic forms and reconverting organic N2 into gaseous N2 • Enzyme synthesis, hormones, vitamins, and other organic substances for plant growth and development • Soil structure modification, influencing porosity, water transitions, and organic matter conveyance, and advancing further root development • Overpowering as well as feeding on soil-borne plant pathogens and plant-­ parasitic nematodes More significance has been accustomed to individuals from soil fauna as pointers of health. This aggregate includes the invertebrate network that lives absolutely or amid something like a period of the existing cycle in the soil (Cardoso et al. 2013; Coyle et al. 2017; Jordán 2009). They assume roles in organizing procedures of terrestrial ecosystems, the disintegration of plant residues, and setting up connections at various dimensions with microorganisms. Hence, they effectively participate in procedures that influence the soil properties and quality, and hence are great indicators of changes in the soil (Lavelle and Spain 2001). For example, nematodes, the simplest metazoan, act as bioindicators of soil health. They demonstrate a high and varied sensitivity to pollutants, and because of their trophic diversity, nematode gatherings do reproduce not only their fate but also the state of the bacterial, fungal, and protozoan communities. Because of such characteristics, they are the potentially remarkable bioindicators for soil disturbance and health (Bongers and van de Haar 1990). A decent variety, biomass, abundance, and thickness of soil fauna have been utilized as indicators of natural or anthropogenic effects on terrestrial ecosystems since these are entirely associated with physical, chemical, and microbiological soil traits (Eggleton et al. 2005; Wardle et al. 2004), and these characteristics of the soil fauna are considered in any prudent methodology utilized for evaluation of the soil health. Associations among plants and soil’s chemical engineers play a critical role in plant network advancement, assorting plant variety, biogeochemical cycling, and supporting general soil structure. Plant roots and microorganisms interact with one

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another through molecular crosstalk, which is useful, impartial, and sometimes detrimental (Kardol et al. 2006). Plants influence the creation of their dirt network, and, consequently, the soil network influences the efficiency and arrangement of the plant network. There are two noteworthy pathways of soil input. One is immediate, using root herbivores, pathogens, and symbionts, and the second pathway is more roundabout, through the impact of the dirt decomposer subsystem on the supply of supplements (Miethling et al. 2000). In many biological communities, plant development is constrained by the measure of nutrients discharged by microbes and parasites, such as ammonium (NH4+), which rely mainly upon the microbial driven disintegration rate. Plants being nonmotile regularly face nutrient deficiencies in their environment, but they have measures to overcome this and obtain micronutrients required for their development and growth. Plant–soil feedback (PSFs) is one such process in which they change the biotic and abiotic potentials of soil, in which they grow, which then alters the plant ability to grow in that soil in the future. Alteration in the measure of quality and quantities of organic substrates flowing into the soil as exudates and litter affects the substrate availability for the microorganism and, eventually, the macroorganisms residing in the soil. Soil invertebrates, along with micro-, meso-, and macrofauna, contribute to plant–soil feedback function, which can lead to the negative, positive, and neutral effects on plant growth. Plant invasion activities are influenced by the PSF, by their impacts on the plant growth. PSFs are mostly involved in the nutrient availability, litter decomposition transfer, soil pathogen accumulation, and interruptions in mutualistic associations in conjunction with soil micro- and mesofaunal populations (Yang et al. 2018 and Zhang et al. 2019). In such similar ways, soil fauna can modulate the soil health that is directly or indirectly related to the associated plant health and can influence the plant invasions and plant network advancement in natural systems by chance, speed, and other different consequences.

5.4

Soil Fauna in Ecosystem Functions and Services

Understanding of how the fauna in soil networks reacts to natural change and how this impacts over-the-ground forms has progressed extensively in the last few decades (Albert et al. 2016; Bragazza et al. 2013; Cheeke et al. 2012; Wurst et al. 2012). A prevalent loss of phylotypes is being observed because of the different management practices, anthropological disintegration, pollution, and widespread urbanization. These have resulting impacts on biological system capacity and ecosystem services, which end up as broadly perceived and identified with bigger concerns such as a reduction in biodiversity, the transformation of habitable lands into deserts, and increased levels of greenhouse gases in the atmosphere (Koch et  al. 2013). An examination by Jeffery and Gardi (2010) showcased prospective susceptibility of micro- and mesofaunal biodiversity and ecosystem services to ecological pressures, together with land management practice. Global trials and amalgamations have kept on tending on the evaluation of the role of soil fauna in ecosystem processes and specifically have prompted expanded proof for their commitment to

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C cycling. Worldwide tests from different geographical areas demonstrate that soil biota are the main controllers of deterioration rates at biome scale (Wall et al. 2008) and indicate that mainly the invertebrate populations in the soil fauna were in charge for approximately 27% normal improvement of litter decay crosswise over biome scales (GarcíaPalacios et al. 2013; Ma et al. 2019). The network of organisms living in soil conveys out an extremely wide scope of biochemical and biophysical forms that directs the working of the soil itself and that can likewise influence the neighboring ecosystems (Maltby et al. 2017; Faber and Van Wensem 2012). Huge numbers of these capacities additionally give basic advantages to human society. The vast majority of these services are supporting services or services that are not specifically utilized by people in any case, which underlie the provisioning of every other service. These incorporate, for instance, nutrient cycling and soil arrangement. Furthermore, soil biodiversity is associated with all the fundamental regulatory services—to be specific, the regulation of atmospheric configuration and temperature, water and air quality, pest and disease occurrence in agriculture and natural environments, and human infections. Soil life forms may likewise control or diminish ecological contamination. At last, soil life forms additionally add to provisioning services that straightforwardly benefit individuals; for instance, the genetic resource of soil microorganisms can be utilized for creating novel pharmaceuticals. Each function adds directly or indirectly up to services. For example, nutrient cycling underlies crop production, while water transfer and storage is affected by soil engineering, and soil biodiversity offers a source of species that may add to pest control, the upgrading of new medicines, or decontamination (Ritz et  al. 2012). Different capacities exhibited by soil and soil biodiversity contribute, in a way, to human prosperity; for example, decomposition of soil organic matter, which adds to carbon storage and climate control. Ecosystem services are characterized as the advantages that individuals get from nature, fundamental for natural wellbeing and human prosperity (MEA 2005). The Millennium Ecosystem Assessment (MA) and the Common International Classification of Ecosystem Services (CICES) classifies ecosystem services into: (1) provisioning, which incorporates the generation of products by biological systems (e.g., fibers, water, food, and energy); (2) regulating, which incorporates the support of a few procedures identified with climate, water and air quality, and pest and disease management; (3) supporting, vital for the execution of all remaining administrations, for example, soil arrangement, nutrient cycling, essential generation, and natural surroundings arrangement; and (4) cultural, which incorporates nonmaterial advantages like amusement, ecotourism, and social legacy. The disintegration of the natural entities by soil fauna is pivotal for the working of a biological community in light of its significant role in giving biological community administrations for plant development and its essential efficiency (Brevik et al. 2019). A comprehensive list of various soil functions performed by soil fauna along with the ecosystem services can be found in Table 5.1. Soil ecosystem services rely upon soil environmental organization (soil biotic and abiotic parts and the connections inside and among them) and soil environment

Kind of service Regulating and supporting services

Decomposition of organic matter; synthesis of organic compounds; mediate transport of water and ions from soil into the plant root; C allocation below ground and its regulation; suppression of pests and diseases Sources of food and medicine; symbiotic and asymbiotic relationship with plants and their roots; plant growth control (positive + negative)

Soil structural maintenance (pest and disease control)

Biodiversity conservation

Soil detoxification; immobilization of nutrients; mutualistic and commensal association; parasite of nematodes and organic matter

Functions of soil biota Soil organization and its preservation; decomposition and mineralization of organic compounds; resource for predatory microfauna; biofilm formation Regulation of soil hydrological processes; associative nitrogen (N)-fixing with legumes; N fixing Gas exchange and carbon sequestration

Attenuation of pollutant

Climate regulation

Soil erosion control

Ecosystem service Water quality

Soil toxicity testing, soil food webs, soil respiration

Emissions of greenhouse gas, phosphorous overflow, nitrate leaching

Macro- and micronutrients, total organic matter, total organic carbon

Indicators Bulk density, porosity, particle size distribution, soil and water retention capacity, water holding capacity

Soil fauna Microfood web; litter transformers; root/rhizosphere biota; N-fixers: mycorrhizae, free-living microbes, microbial pathogens; root herbivores: bacteria, archaea, fungi, actinomycetes; Protista: predators (bacterivores); Nematoda: plant feeders, predators (bacterivores, fungivores); Collembola: saprovores, predators; Acari: saprovores, predators; litter transformers: mesofauna— Enchtriaeids, earthworms, termites Ecosystem engineers: macrofauna— earthworm, macroarthropods, burrowers, saprovores, Arthropoda, Enchytraeids; biocontrollers: predators, parasites (hyper), microbial pathogens, root herbivores

Table. 5.1  Relationship between soil ecosystem functions and services with relevant indicators and responsible soil fauna

Leal et al. (2014), Pringle et al. (2010), Shi and Shofler (2014), and Maleque et al. (2009)

Jouquet et al. (2014); Evans et al. (2011); Leal et al. (2014)

Hope et al. (2014), Baron et al. (2014) and Wu et al. (2010)

Hammer et al. (2016) and Metcalfe et al. (2014)

References Metcalfe et al. (2014)

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Food, water, fiber, and energy supply

Physical or experimental use; intellectual representations

Provisioning services

Cultural services

Consumption of organic matter; create channels in soil and litter for movement; predators of other soil and surface-dwelling organisms

Food quality and storage, plant physiology, crop productivity, creative landscape, leisure activities Beautiful landscape, participation in leisure activities, vital actor awareness

Microfood web; microflora: bacteria, fungi; microfauna: protozoa, nematodes, microarthopods; litter transformers: megafauna—moles, little rodents, reptiles

Vidal et al. (2014) and Morley et al. (2014)

Rodriguez et al. (2006), Macadam and Stockan (2015), Sehnal and Sutherland (2008) and Dzerefos and Witkowski (2014)

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capacities (regular procedures happening in soil). In the case of soil, water, and air, air compartments are interdependent, and their quality and maintainability are reliant on one another. Soil environment structure is in charge of the adjustments in individual life forms, and hence their role and capacity in soil modification and consequently in the biological community assembly. Soil biodiversity in this way manages soil structure and capacities (Morgado et al. 2018).

5.5

Conclusions and Future Studies

Earth environmentalists and soil modelers have generally depicted the occupants of soil as a black box named as “soil fauna” or “decomposers or detritivores,” recognizing the fact that they reuse the stored dead material. The soil is a standout among the various living spaces on earth and contains a diverse collection of living organisms; but, the opaqueness of this world has extremely constrained our comprehension of their functional commitments to soil forms and ecosystem flexibility. Conventional scientific categorization, given morphological and anatomical angles, is getting to be supplanted by molecular techniques (e.g., with marker gene-based methodologies). Nonetheless, this might be impracticable in numerous natural or ecological situations, and therefore the larger part of the present learning still contributes little to our comprehension of their roles in ecosystem functioning. The present chapter has investigated the reasons why soil fauna is considered for their inherent, useful, and functional qualities. Inherent reasons alone legitimize examination into these different and complex networks and their preservation through natural surroundings and suitable land management practices to address the issues for forthcoming generations. It is recommended that the significance of soil fauna remains an oddity in light of the fact that on one side broad research has demonstrated that they have significant consequences for soil biophysical forms at the scales at which the organisms are active, and on the other side these impacts are once in a while obvious at plot, biological community, and ecosystem scales. Three components are proposed to clarify this mystery. Firstly, that in very differing networks the “signal” of specific soil fauna impacts is concealed by the “noise” from other biophysical occasions that add to similar properties and procedures (e.g., carbon and nitrogen mineralization, soil structure). Secondly, that numerous procedures made by soil fauna have “sink” and “source” elements that can cancel the signal of these nearby impacts at bigger spatial scales. Thirdly, that at enormous temporal and spatial scales, biophysical parameters are utilized as rate determinants of biological system forms and the structure of above or subterranean networks is once in a while raised. However, there are conditions in which the environments are in transitional states, or in which natural occasions synchronize with activities of soil fauna when roles of soil fauna end up clear at the plot and environment level. Further examination into these procedures could define circumstances in which soil fauna are key determinants of biological system functions or ecosystem processes and increase acknowledgment of the soil fauna by different disciplines.

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6

An Insight into Current Trends of Pathogen Identification in Plants Vinay Kumar, Vinukonda Rakesh Sharma, Himani Patel, and Nisha Dinkar

Abstract

Worldwide, plant diseases have caused major economic losses in the agricultural industry. Food security is a major issue to the rising global population.  Plant health monitoring and the early detection of pathogens are important in decreasing the propagation of diseases and providing the best strategy. To reduce the damage caused by old and new pathogens, and to speed up the management and reduction of crop loss, a fast and reliable detection method in combination with decision support systems is essential. New tools and technologies were developed for both detection and diagnosis, often substituting old methods to make them quicker, more accurate, and precise. With the rising global population, there is need to boost crop production and protect the crop from seed to market. There is also need to use the latest technology for rapid and precise diagnosis of plant diseases to minimize losses for sustainable production. In addition to the traditional visual screening for symptoms, nucleic acid and serological-based tools will provide precise and rapid detection and diagnosis. Remote sensing technology, along with spectroscopy, will help in the capture of high spatialization of results, and can be very useful to identify primary infections quickly. Handheld antibody-based immuno-biosensor also helps the rapid detection of plant diseases. This chapter enlightens on the various recent technologies in plant

V. Kumar (*) · V. R. Sharma Genetics and Plant Molecular Biology, CSIR-National Botanical Research Institute, Lucknow, Uttar Pradesh, India Academy of Scientific and Innovative Research (AcSIR), Ghaziabad, Uttar Pradesh, India H. Patel Birbal Sahni Institute of Palaeosciences, Lucknow, Uttar Pradesh, India N. Dinkar Department of Biotechnology, Khandelwal College of Management Science and Technology, Kalapur, Bareilly, Uttar Pradesh, India © Springer Nature Singapore Pte Ltd. 2020 M. K. Solanki et al. (eds.), Phytobiomes: Current Insights and Future Vistas, https://doi.org/10.1007/978-981-15-3151-4_6

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pathogen identification for sustainable and effective crop production, and the safeguard of the crop produce. Keywords

Pathogen identification · Molecular diagnostics · PCR · Plant pathology · Plant diseases

6.1

Introduction

Due to increasing population and globalization, food security, and prevention of the spread of invasive pests/pathogens, accurate identification and diagnosis of plants are very important to protect available crop produce. Plant pathogens causes significant losses in plant yield. Enormous economic losses due to wheat rusts and Fusarium head blight claimed US $5 and US $3 billion/year, respectively (Schumann and D’Arcy 2009). Precise, sensitive, and special diagnoses are necessary to manage plant diseases efficiently and economically. Identification of plant diseases have evolved from visual inspection to the use of high-profile serological tools such as the enzyme-linked immunosorbent assay (ELISA), and molecular methods like polymerase chain reaction (PCR). MLO-7 gene in the grapes against powdery mildew disease, which ultimately increase the precision for the latest technologies such as CRISPR (clustered regularly interspaced short palindromic repeats) in plant disease studies, has become possible through the application of biotechnology and bioinformatics in plant pathology (Malnoy et al. 2016). Although progress has been made about all aspects of plant disease diagnosis, there is a need for increased sensitivity and specificity of molecular studies for rapid detection and diagnosis. This chapter describes briefly the different techniques used for diagnosing plant diseases and their contribution to the current challenges for global food security.

6.1.1 Microbiome Diversity The diversity of the plant microbes is defined as the number of microbe species present in the particular ecological area and relationship between them with their ecological, environmental conditions (Vos et al. 2016). Nowadays, a different type of molecular methods was used in the detection of microbes present in the sample. Firstly we collect the sample and isolate the DNA/ RNA/protein/lipids and then follow the different methods, viz., PCR, qPCR, MALDI-TOF MS, electrospray, and ionization mass spectrometry, for the assessment of diversity present in the sample (Table 6.1). Here, Table 6.1 discusses some molecular techniques for plant disease diagnosis.

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Table 6.1  List of different techniques involved in the detection of plant microbes with their advantages and disadvantages Detection methods Visual detection

Polymerase chain reaction-based methods

Conventional PCR

Portable rapid cycler PCR Nested PCR

Multiplex PCR

Reverse transcriptase PCR

Real-time qPCR

Serial analysis of gene expression (SAGE)

Merits Simplest methods

Demerits Lack of sensitivity in detecting that occur in low concentration, asymptomatic

Specific primer for particular species produces precise and rapid results Identification of plant disease at on-site Utilization of two pairs of primers raises yield and accuracy of desired DNA amplification Resources and time rescued by using the various set of primers in PCR reactions It is more accurate than standard PCR and produces the quantitative data

More costly and necessitate more labor

No requirement of post-­ amplification reaction and it is an automated process Reference knowledge of the genome is not required

Pricey and deficient in robustness

References Ali et al. (2019), Gomez et al. (2019) and Cooke and Cacciola (2007) Milijasevic et al. (2006) and Walcott and Gitaitis (2000) Love et al. (2012)

More chances of contamination due to two times amplification reactions

Lee et al. (1997) and Bereswill et al. (1995)

Primer and probe interference reduces the sensitivity

Rico et al. (2003) and Fegan et al. (1998)

Information about every test is difficult and involves costly materials and chemicals Pricey and difficult in owing to concurrent detection of thermocycling with fluorescence Accuracy of the tag sequences

Liu et al. (2019a, b)

Schaad et al. (2007) and Salm and Geider (2004)

Tarasov et al. (2007)

(continued)

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Table 6.1 (continued) Detection methods Northern blotting DNA/RNA probe-based methods

Merits Identification of size of RNA

In situ hybridization

It required more supply of tissue

Fluorescence in situ hybridization (FISH)

It can be used in nondividing cells

Post-­ amplification technique

Microarray Macroarray

It is high-­ throughput tool and allows identification of various pathogens

Isothermal amplification-­ based methods

Loop-mediated isothermal amplification (LAMP) Rolling circle amplification (RCA) Nucleic acid sequence-based amplification (NASBA)

Fast, accurate, and extremely specific

RNA-sequence based next-gen. sequencing The RNA interference (RNAi)

Simplicity, efficiency, tunability There is no need for expensive equipment, and also it is better than RT-PCR Specificity and sensitivity higher

It is potential to investigate thousands of genes concurrently

Demerits It applies to the very specific sample of the gene sequences It is very complex to detect the target of sequences with low copies of DNA or RNA It is essential to identifying the target DNA sequences It does not differentiate the living and non-living cells analysis

Primer formation is more careful binding only on the specific pathogen –

Sample reaction temperature is 42 °C, and it cannot be increased because it depends on enzymes It requires more costly tools and information for the data analysis Diversity and incompleteness of knockdowns and latent in nonredundancy of chemicals

References Yin et al. (2019) and Boccardo et al. (2019) Ellison et al. (2016) and Tanaka (2009)

Sidra et al. (2017) and Ratan et al. (2017) Osmani et al. (2019), Leborgne and Bouhidel (2014) and Sato et al. (2010) Almasi et al. (2013)

Gomez et al. (2014) Gabrielle et al. (1993)

Dawei and Peng (2014) and de Jonge et al. (2012) Machado et al. (2017)

(continued)

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Table 6.1 (continued) Detection methods Spectroscopy MALDI-TOF MS

Antibody

Demerits Difficulty in distinguishing some organisms that are closely related genetically Capable of directly analyzing which are nonvolatile, polar, or thermally labile Better sensitivity required

References Bruker (2016)

Fang et al. (2014)

Volatile compounds (GC-MS)

Highly indicative, accurate, high specificity

Quartz crystal microbalance immunosensors (QCMI) Agriculture nanobiosensors

Real-time analysis possible

Real-time analysis possible

Just beginning, trouble of reproducibility, and measurement errors

Tissue blot immunoassay (TBIA) ELISA

Quick and simple to use

Costly

It can manage a large amount of samples in the same time and produces more accurate results Concurrently identification and quantification of various pathogens in a consistent manner High sensitivity, real-time analysis possible

Pre-enrichment is required for more surface antigens and more highly skilled manpower required More investment and very less information of this tools

Kanakala and Kuria (2018)

Limits for detection, trouble of reproducibility, and measurement errors

Syed and Ahmad (2013) and Kumar et al. (2007)

Flow cytometry

Quantum dots (QDs)

6.2

Merits Much faster, rapid turnaround time

Huang et al. (2014) and Zan et al. (2012) Etefagh et al. (2013) and Dubas and Pimpan (2008) Chang et al. (2011)

Fang and Ramasamy (2015) and D’Hondt et al. (2011)

Toolbox for Diagnosing Plant Pathogens

The knowledge of the physiological method of interaction is lacking for many years between host and pathogen for many systems of pathogens (Table 6.2). Recently, quantitative high-performance imaging methods have been developed to phenotype plant growth and development (Mutka and Bart 2015). The following methods help to study the changing physiology of plants due to pathogens that further help in the development of mechanisms for disease symptoms.

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Table 6.2  List of important fungal, bacterial, and viral pathogens affecting crop plants with their diseases, host, and percentage of crop loss S.no. Pathogen A Fungal 1 Fusarium oxysporum

Disease

Host

Crop loss

References

Wilt

Nearly 80%

Debbi et al. (2018)

2

Blumeria graminis

Up to 45

3

Botrytis cinerea

Powdery mildews Gray mold

100 different hosts (mostly horticulture crops) Poaceae crops

50–100%

4

Colletotrichum spp.

Anthracnose

5

Magnaporthe oryzae B.C. Couch

Blast disease

6

Melampsora lini

Rust

200 crop hosts worldwide Economically important crops, especially fruits, vegetables, and ornamentals Poaceae crops and their wild relatives Flax

Zulak et al. (2018) Rupp et al. (2017) Han et al. (2016)

7

Head blight

Wheat and barley

Up to 70%

Blotch

Wheat

30–50%

9

Fusarium graminearum Mycosphaerella graminicola Ustilago maydis

Smut

Corn

80%

B 1

Bacterial Agrobacterium tumefaciens

Crown gall tumor

140 species of eudicots

2

Xylella fastidiosa

Pierce’s disease of grapevine (PD), citrus variegated chlorosis (CVC), and almond leaf scorch disease (ALSD)

Horticulture crops and especially grapes

Considerable economic loss Serious losses in grape production

8

Up to 100%

10–30%

Yoshida et al. (2016)

~80%

Nemri et al. (2014) Yang et al. (2013) Simón et al. (2012) Dean et al. (2012) Dean et al. (2012)

Kerpen et al. (2019) Kyrkou et al. (2018)

(continued)

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Table 6.2 (continued) S.no. Pathogen 3 Erwinia amylovora

Disease Fire blight

4

Cassava bacterial blight

5

6

7 8

Xanthomonas axonopodis pv. manihotis Pseudomonas syringae pathovars Pectobacterium carotovorum (and P. atrosepticum) Xanthomonas oryzae pv. oryzae Ralstonia solanacearum

9

Xanthomonas campestris pathovars

C 1

Virus Tomato yellow leaf curl virus (TYLCV) Tomato spotted wilt virus (TSWV) Brome mosaic virus (BMV) Potato virus Y (PVY) Cauliflower mosaic virus (CaMV) Cucumber mosaic virus (CMV) Tobacco mosaic virus (TMV)

2 3 4 5

6 7

8 9

Plum pox virus (PPV) African cassava mosaic virus (ACMV)

Host Apple, pear, quince, blackberry, raspberry, and many wild and cultivated rosaceous ornamentals Tubers

Crop loss Serious losses in pome production

References Aćimović et al. (2015)

12–100%

Blight, canker, brown spot, etc. Soft rot, blackleg

Mostly horticultural crops Mostly potato

40%

LÓpez and Bernal (2012) Mansfield et al. (2012)

Serious

Nykyri et al. (2012)

Bacterial leaf blight Bacterial wilt

Poaceae crops

Up to 22.5%

Very wide range of potential plants 57 families of dicotyledons and mostly cruciferous crops

25–75%

Soto-­Suárez et al. (2010) Artal et al. (2012)

20–45%

Hayward (1993)

Wide host range (>800 plant species) Around 500 species of crops Poaceae crops

Up to 60%

Ding et al. (2019)

Up to 100%

Solanaceae

50–80%

Brassicaceae family

25–59% loss

Gupta et al. (2018) Ding et al. (2018) Hussain et al. (2016) Schoelz et al. (2015)

More than 40 families Many economically important crops Pome fruits

Up to 60%

Tubers

30–100%

Black rot

Leaf curl

Spotted wilt Mosaic of grasses Necrotic lesions Cauliflower mosaic virus Mosaic Necrotic local lesions Plum pox Cassava mosaic disease

Up to 20%

20–80%

20–40%

Phan et al. (2014) Scholthof et al. (2011) Cambra et al. (2006) Fargette et al. (1988)

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6.2.1 Visual Detection One of the simplest methods for plant pathogen detection was a plant germplasm visual inspection and subsequent selection of healthy matter. Disease scaling based on visual symptoms is being acceptable with accuracy since the last 80  years (Martinelli et  al. 2015). Different methods can be used for the visual inspection including visible illumination, chlorophyll fluorescence imagery, infrared imaging, and electromagnetic spectrum imaging (Cooke and Cacciola 2007; Bock et  al. 2010; Li et al. 2014a, b; Odilbekov et al. 2018). The environmental and biological factors have a strong influence on these methods. Traditional methods for measuring the severity of the disease are not reliable for population estimating diseases lack standardization and procedural (Nilsson et al. 2011). In asymptomatic plants and less virulent pathogens, visual inspections may not be helpful; many hosts remain symptomatic (Mutka and Bart 2015; Ali et  al. 2019; Liu et  al. 2019a, b; Gomez et al. 2019).

6.2.2 Serology-Based Diagnostics Phenotypic observation of plants with pathogenic symptoms would require extensive experience in the diagnosis of plant diseases and isolation of the disease. But for all attempts, the exactness of the same cannot necessarily be the same. Furthermore, the detection of the pathogens in asymptomatic samples or seeds is very likely to be diagnosed properly. The precise identification and an adequate diagnosis procedure would contribute more promisingly to plant health management. Through inventions of precise methods of detection, better management strategies are developed, and then, the rapid detection tool, in particular, an onsite handy one, definitely helps to achieve management success. A handy detection kit for potato viruses has been developed recently, which growers can use easily in the field (Ansar and Singh 2016). No artificial cultivation of plant pathogens like viruses and obligate pathogens causing rusts and powdery mildew and downy mildew diseases was possible. To address this problem, there were developed serologic assays, which are also used to identify other plant pathogens (Caruso et  al. 2002). Serological pathogens of plants involve identifying disease based upon color-changing antibodies of the assay. The antibodies consist of immunoglobulin (Ig) proteins produced within the animal body (mammalian), which in general include foreign proteins, complex carbon dioxide, multiple nucleotides, or lipopolysaccharides. As we know, each antigen binds to a particular antibody. The serological method most commonly used is ELISA (enzyme-linked immunosorbent assay) as previously developed for plant virus detection (Clark 1981).

6.2.2.1 Enzyme-Linked Immunosorbent Assay (ELISA) ELISA is done with polystyrene plates capable of binding enzyme-substrate reaction antibodies or proteins (Corning Life Science 2001; Luminex 2010). The enzyme-substrate response must be optimized in the timing and development

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conditions to produce accurate and replicable results. ELISA is a popular test for the detection of plant pathogens present in plant resources and insect vectors (Clark and Adamas 1977; Naidua and Hughes 2001; Webster et al. 2004). Disease levels are observed on the bases of optical density in ELISA (Corning Life Science 2001; Webster et al. 2004). ELISA has benefits because it is more accurate; a big amount of tested materials can also be evaluated using a small number of antibodies to detect illnesses and a semiautomated process (Vemulapati et al. 2014; Naidua and Hughes 2001). Specific antibodies against the target pathogen have been developed (Torrance 1998). This technique is utilized for the identification of the various types of virus, i.e., Citrus tristeza virus (CTV), potato leaf roll virus (PLRV), potato virus X (PVX), and potato virus Y (PVY) (El-Araby et al. 2009; Sun et al. 2001). Since ELISA is a test based on antibody antigens, the availability of antibodies that react properly to the target agent is considered very important. ELISA often provides erroneous diagnostic because of false positive, which results primarily from unspecific or cross-reactive reactions with certain sample factors (Kfir and Genthe 1993). Several strains with a clear different symptom may be responded to by the antibody used in ELISA due to the absence of great specific places to bind. Consequently, much related to different types of virus are not properly distinguished by ELISA (Boonham et al. 2014). Different type of additives were includes in extraction buffer for increased in ELISA sensitivity (Fegla and Kawanna 2013). When compared to molecular methods, ELISA is generally less sensitive. For these reasons, the utilization of ELISA in the way of diagnosis appears to progressively fall down, even when ELISAs have been used in the most up-to-date diagnostic purposes.

6.2.2.2 Tissue Blot Immunoassay (TBIA) Tissue Blot Immunoassay (TBIA)  is similar to the principle of ELISA in which antibodies are functional; TBIA has a similar consistency to ELISA to detect plant pathogen like that virus (Hančević et al. 2012). The main difference is that polystyrene plate is working as a platform for ELISA, while nitrocellulose and nylon membranes are treated with TBIA; that’s why this assay is also known as TIBA or TBIA (Webster et al. 2004). Similar to ELISA, TBIA is also required for the particular antibody to find clear false positive and false negative. Therefore, TBIA has huge advantages over ELISA in different conditions such as time, money, sensitivity, and expediency of detection. In TIBA, we have detected a various number of viral diseases in which some are here, i.e., bamboo mosaic virus (BoMV), bean yellow mosaic virus (BYMV), CTV, Cymbidium mosaic virus (CyMV), papaya ringspot virus (PRSV), sweet potato feathery mottle virus (SPFMV), and tomato spotted wilt virus (TSWV) (Bove et al. 1988; Eid et al. 2008; Hančević et al. 2012; Lin et al. 1990; Makkouk and Kumari 2006; Shang et al. 2011; Webster et al. 2004). 6.2.2.3 Flow Cytometry (FCM) Flow cytometry is a laser-based optical method. The technique is widely used in the fields of cell count, cell sorting, biomarker, and protein detection (O’Donnell et al. 2013). Many samples can be processed simultaneously via electronic detection

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devices, and the technique simultaneously measures many parameters (Fang and Ramasamy 2015). Flow cytometry is widely used to evaluate microorganisms in the processing of food in drinking and marine water. FCM is not currently widely used as an instrument for research and detection in plant pathology; however, it can be used to test the total DNA content in bacterial, oomycete, and fungal disease agents and check pathogen viability; FCM can be used in the field of plant pathology for multiplexed path detection (D’Hondt et al. 2011). Flow cytometer rating is highly precise and purifies little or complex populations, but some of them are not fast enough to achieve the desired results even for a high-speed rating, and it costs more than the alternatives such as radioimmunoassay and ELISA.

6.3

Molecular Methods

Molecular methods of diagnosis of diseases are one of the remarkable sciences that are fast-growing and have the potential to revolutionize numerous scientific research, innovations, healthcare, and agriculture disciplines.

6.4

Genomics-Driven Diagnostics

6.4.1 Conventional PCR The innovation of PCR got an incredible boom in the field of plant pathology. This tool permits amplification of specific DNA sequences in lots of duplicates by utilizing specific primers (Cha and Thilly 1993). At first, PCR was very explicit for the detection of infections brought about by microscopic organisms, i.e., bacteria, fungi, and virus. Presently, this tool is broadly utilized for the detection of the pathogen from the infected plants (Fig.  6.1). Occasionally, efficiency is influenced by sampled inhibitors (Fang and Ramasamy 2015). To resolve this problem in plants, cetyltrimethylammonium bromide (CTAB) can be used to add particular treatments with different chemicals and enzymes. A few different techniques are available to decrease PCR inhibitor effects. In the case of DNA isolation through the phenol-­ chloroform method, as a substitute for ethanol precipitation and silica bed, recovery of DNA can be done by purification (Mancini et al. 2016). Also, it can detect plant pathogens; PCR technology requires first to start the DNA replication procedure that might decrease the convenient application for disease field sample technology. Sometimes a single pair of primer does not give accurate results so that its limiting effect is overcome by DNA samples and nested primers. (Compton 1991). The detection of P. granati was established using nested PCR (Yang et  al. 2017). Presumably, this methodology gives exceptionally explicit outcomes. However, it is a lot very expensive and required much effort (Sidra et al. 2017).

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Fig. 6.1  PCR-based method for identification of microbes

6.4.2 Nested PCR A high degree of specialty and sensitivity can be found using nested PCR (Sidra et al. 2017). For example, “Grote et al. (2002) reported that relative study on sensitivity and specificity of phytophthora nicotianae using both simple and nested PCR” revealed that the nested PCR sensitivity is 1000 times the detection of a single PCR. In this procedure, primers can be utilized for the amplification of large DNA sequence through the two continuous cycles, the afterthat sequence of amplified product works act as a specific sequence for second times by the use of two internal primers. In nested PCR, tremendous risk of contamination is assessed even though, in separate tubes, two amplification cycles should be performed. There is, therefore, the probability of false adverse population outcomes, and heavy labor is a significant defect (Rahman et al. 2013). Laboratories must take certain tough measures for the use of different instruments and space for each PCR cycle to conquer such borders (Trtkova and Raclavsky 2006). Two Phytophthora species P. palmivora and P. parasitica have been identified using this PCR (Tsai et  al. 2006). Likewise, P. cactorum was particularly identified in strawberry infected plants through utilizing this technique (Bhat and Browne 2010), as well as rapid detection of Cylindrocladium scoparium on eucalyptus (Qiao et al. 2016). For the identification of Candidates Liberibacter asiaticus attached with citrus Huanglongbing (Hong

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et al. 2019), another report says that nested PCR can be used for detection of Lyme disease spirochete, Borrelia burgdorferi, in ticks (Wills et al. 2018).

6.4.3 Multiplex PCR This method is utilized to demonstrate in less period as well as less money by utilizing few sets of preliminaries for a similar response to permits synchronous recognition of various focused on successions of DNA (Hyun et al. 2017). The method has such extraordinary significance of enormity in plant disease when crops are contaminated with many pathogens. Distinctive parts are clearly to target pathogenic parasites where at the same time enhanced and identified based on their molecular weight on agarose gel electrophoresis. DNA combining accuracy was unequivocally influenced by amplicon measure. To maintain a strategic distance from this entanglement, groundworks must be structured cautiously along with the comparative center and strengthening (Dasmahapatra and Mallet 2006). At present, lock tests (padlock primers) are utilized for the detection of pathogenic growths. This system has been utilized to the concurrent ID of parasitic pathogens, for example, F. oxysporum, B. cactivora, P. nicotinae, and P. cactorum, that key illness in joined cacti (Cho et al. 2016). Detection of various citrus disease-causing viruses in Jeju Island (Hyun et al. 2017), multiplex reverse transcription PCR assay for simultaneous detection of six main RNA viruses in tomato plants (Wu et al. 2018).

6.4.4 Portable PCR Systems Fast PCR can manufacture a fully mobile configuration that will not just facilitate plant pathologists to carry out great efficiency with consistent experiment testing, but it might be significantly similar to downstream methods, i.e., those mandating in situ genomics detection tools. Palm PCR, manufactured in Korea by Ahram Biosystems, is easy to use, accurate, and high-competence thermal cycler (Love et  al. 2012). Although it’s small in size, this control tool provides tremendously well-defined and rapid amplification for different types of DNA materials (Monis and Giglio 2006). The amplification of the DNA to a sufficient amount is less than 25 minutes for the optimal detection in the agarose gel electrophoresis. The transferable way provides a greatly efficient easy-to-handle way for the learner and experienced academician to perform a different type of PCR tests. Koo et  al. (2013) reported the successful identification of the six diverse fungal and bacterial plant pathogens in the sample. Twista quantitative and portable real-time fluorometer are personalized tools produced to examine reactions to recombinase polymerase amplification (RPA) comparable with a different type of detection systems and the latest technology in DNA identifications, very high speed, easy to carry, and user-friendly with super quality. Twista RPA fluorometer provides urgently rapid diagnosis, enabling

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appropriate on-time therapy compared to usual microbiological test requiring at the minimum an hour and molecular assays typically requiring consolidated tools (Surrette et al. 2018).

6.4.5 Real-Time Polymerase Chain Reaction (RT-PCR) Real-time PCR invention has developed more amount of modification in its protocol. A portion of maximum changes has extended the utility and detection quality of this PCR in numerous natural as well as therapeutic fields (Tang et al. 1997). These tools are insufficient to differentiate the living and dead parasites. PCR cannot differentiate between dead and living parasites. The DNA can be obtained from the liver and circulating DNA from other cells or bodies. The addition of a PCR test aimed at Leishmania-specific mRNA in a householder gene should make a difference between living and dead parasites (Bretagne et al. 2001). The development of RT-PCR overpowers this limitation. Contamination in mRNA is present in the dead cell; therefore, RT-PCR can detect the presence of mRNA in the cell (Capote et al. 2012). In this regard, RNA is conversely deciphered into cDNA by irregular groundworks and real-time compound and after that intensified by various PCR methods. In this way, RT-PCR is utilized to recognize and analyze the RNA-containing (retroviruses) contaminations. The finding of RNA-containing infections can help make or check the practicality of antimicrobial inoculations or treatment. For example, it can be utilized for evaluation of Fusarium graminearum growths to reason Fusarium early curse sickness within grains, for example, wheat, grain, and oat (Brown et al. 2011). Cryphonectria parasitica can be detected early using RT-PCR (Chandelier et al. 2019). Concurrently, it can detect the various pathogens of potato (Nikitin et al. 2018). Recently, quantitative real-time PCR is a technique which affects microbial ecology greatly. The qPCR is a very sensitive technique to quantify the microbial population within the ecological sample (Trung et al. 2011). In short, qPCR amplified the specific sequence of nucleic acids and also calculates the sample amount of DNA.  The fluorescent marker (SYBR Green)  present at the end of the reaction detected by the PCR instrument. SYBR Green I and high-resolution melt dyes (LC Green, EvaGreen, BEBO, and SYTO9) can link between the dsDNA and emit the fluorescence at 494 to 521 nm wavelength. Similarly, another way used in the qPCR analysis, i.e., TaqMan probes, works on a third oligonucleotide during annealing. The probe is made up of two molecules: (1) reporter and (2) quencher. When these two come together, then they repress the fluorescence of reporter in the reaction of DNA amplification. Also it generates the signal intensity with the amount of target DNA amplification. Detection of the pathogen such as Phytophthora infestans from the potato (Hassain et al. 2014; Li et al. 2014a, b; Clement et al. 2013) and Verticillium dahliae, Colletotrichum acutatum, and C. gloeosporioides from the strawberry (Bilodeau et  al. 2012; Garrido et al. 2009) is through qPCR.

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6.4.6 Serial Analysis of Gene Expression (SAGE) Sequential examination for quality articulation was thorough based on grouping strategy for the quantitative quality articulation data that permits recognizable proof in numerous transcripts (Moreno 2003). SAGE is based on sequencing data of 15 bp or more nucleotides and comparability of successions beside accessibility of genome groupings to locate the relating communicated qualities (Velculescu 1995). It can utilize two examples that are bound and signed with the different preliminaries, and it’s intensified. At that point, concatemers are shaped by the sticky finishes through the expulsion of groundwork. In sequencing of the cloned vector using the computational investigation, SAGE has a few downsides. In the first place, it needs mRNA in an extensive amount. Second, now and then the 15 bp tag isn’t sufficient to explicitly recognize the quality of birthplaces with the more mind-boggling genomes. Thomas et al. (2002) reported that in the profiling of transcript of mildew pathogen Blumeria graminis in barley, SAGE is used, and another scientist also reported that gene expression of Nicotiana tabacum in Rhizoctonia solani is through SAGE (Portieles et al. 2017).

6.4.7 Sequencing-Independent Methods The probe of DNA/RNA strategies is utilized to analyze plant infections caused by the microorganisms, for example, fungi with extraordinary sensitivity and speed (Sidra et al. 2017). This innovation is considered as the spine to a large portion of the present information. In these techniques, the probe shall be used without its amplification for the testing of nucleic acid. Samples are the shortest single-stranded DNA sequence that is named with chemiluminescent molecules or radio isotopes, for example, 32P, 33P, and 35S (Sidra et al. 2017). For instance, engineered zinc finger proteins do not require targeted amplification for the detection of specific pathogen DNA (Kim and Kim 2016). It is utilized for the recognition of similar sequencing present on specific DNA. In traditional techniques, DNA probes is utilized for the most part as an option to PCR for the recognizable proof of microorganisms such as fungi. Be that as it may, in ongoing techniques, these are for the most part utilized related to PCR (McCartney et al. 2003; Khater et al. 2019). Engineered zinc finger proteins and pathogen targeted DNA immobilized on a chip of polymer (Ha et al. 2018; Guixia et al. 2019).

6.4.8 Northern Blotting or Northern Blot This technique is also called as RNA smear technology and is generally used for the exchange of RNA onto a bearer for the recognizable proof of pathogenic growths utilizing the quality articulation (Zimmers-Koniaris 2001). The northern blot is equivalent to the southern smear apart from RNA material is utilized rather than DNA (Qi and Yang 2002). Right off the bat, the RNA from each tissue ought to be

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purged be inspected the statement of the quality of intrigue. RNA molecule was separated on the agarose gel electrophoresis. In this gel, litter molecule moves faster than a higher molecule; in this way, higher molecules present well as compared with the litter molecule (Kim et al. 2010). Hence every RNA molecule keeps its position regarding every single another particle (Berg 2007). The way is present to do a radioactive test to hybridize its related grouping molecule. After that, the channel is put for autoradiography to build up the film. At last, a band ought to show up on it, if both tests have hybridized a section of RNA atom on the channel. To start with, the situation of groups at smudge gives RNA approximation, but a measure of RNA is known; then they will give a guess to coding limit of transcripts as well as the extent of protein to which it recognized. Right from the beginning, the danger mRNA corruption amid electrophoresis is the primary impediment in the smudging system. Besides, recognition with numerous tests is hazardous. The affectability of the northern smudging strategy is low contrasted with RT-PCR. Magnaporthe grisea was perceived in rice plants through utilizing ongoing PCR and northern blot technique (Qi and Yang 2002). Agrobacterium-infiltrated place can be detected with the presence of more amount of GFP mRNA and siRNA through northern blot techniques (Yin et al. 2019; Boccardo et al. 2019).

6.4.9 In Situ Hybridization In 1969, exploration of nucleic acids by in situ hybridization was first revealed (Gall and Pardue 1969). In situ hybridization is likewise called the hybridization histochemistry. It gives precious data to recognizing and listing the parasites. In these method, the ssRNA test is utilized known as riboprobes and 35S. It has an extraordinary closeness to northern blotting. These two methods rely upon hybridization of marked tests of DNA/RNA to the comparative groupings of mRNA molecule. These strategies vary in the utilization of beginning material. On account for northern smudge, the part of tissue digest is utilized as beginning material, while in situ hybridization histological area is utilized. Notwithstanding utilizing the immediate hybridization, the recognizable pieces of proof utilizing signal hybridization are most productively acquired after the organism’s development or its natural intensification (Jensen 2014). The preferred primary standpoint of this innovation is the most extreme utilization of tissue, for example, clinical biopsies and refined cells. Several unique hybridizations can be done in a similar tissue. Tissue libraries can be arranged by putting away in cooler for future use. There are various techniques for performing in-situ hybridization, for instance, testing with counterfeit oligonucleotides copy of DNA and RNA. These strategies give the most powerless and efficient outcomes. Tests may be named according to radioactive or nonradioactive nucleotides; after these tests, 35S riboprobes are a very delicate strategy for the ID of mRNA (Hayden et al. 2002). ISH was used to locate specific chromosome DNA sequences using radioisotope-­labeled samples (Gall and Pardue 1971; Zeller et al. 2001). It was later used for detection of viral particles and mRNA high copy in cultivated cells and

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sectional tissue, so that gene expression patterns could then be located (Brahic and Haase 1978; Zeller et al. 2001). It is used for pathogen visualization in host plant tissue, using ISH technology (Tanaka 2009). In situ hybridization has a few entanglements. Right off the bat, radiolabel tests are in all respects expensive and risky materials. It must be dealt with, transported, and discarded in all respects cautiously. A drawback of utilizing in situ hybridization procedure is the trouble in distinguishing focuses on with contains a low copy of DNA and RNA molecules (Qian and Lloyd 2003). It can be used for identification of various parasites, i.e., Blastomyces dermatitidis, Coccidioides immitis, Cryptococcus neoformans, Histoplasma capsulatum, and Sporothrix schenckii (Hayden et al. 2001). This type of hybridization can be used to imagine the difficulty in plant tissue of the rust organism, as well as it can be utilized for confinement region that is present in plant partition in rust fungi (Ellison et al. 2016).

6.4.10 Fluorescence In Situ Hybridization (FISH) Because of the disadvantage of radiolabeled probe-based hybridization, the FISH technique has emerged, which is used for the speedy characterization of microorganism such as fungi (Sidra et al. 2017). This technology offers superior speed, resolution, and security and smoothens the way for simultaneous and quantitative phylogenetic analysis of multiple targets (Tsui et al. 2011). Besides this, FISH is also an essential type to identify break down in the spatial association of fungal networks. Specific DNA sequence on chromosomes is detected using this cytogenetic technique (Ratan et al. 2017). The fluorescent probe is used in FISH which single binds those parts of the chromosomes, which shows a higher quantity of similarity. Fluorescent samples are established throughout the sample length by an enzymatic fuse of altered fluorophore base (Baschien et al. 2001). Conventional systems for detection of microorganism necessitates that cells should be effectively isolating (Ainsworth et al. 2006). However, for non-diving cells, FISH can be used, making it a highly resourceful technique. It is possible to recognize non-dividing cells by their low fluorescence intensity level. It is possible to use a different type of samples, for instance, an allele-specific sample, a centromeric repeat sample, and an entire chromosome sample. Many of them have various implementations. In FISH probe, preparing ready procedure is confounded because it is important to tailor probe to recognize the particular sequence of DNA (Volpi and Bridger 2008).

6.4.11 Microarray A microarray is a technique that is used simultaneously to detect the expression of thousands of genes. It is a microscopic slide that is printed in defined positions with thousands of tiny spots with each spot referring to the known DNA sequence or gene, and these slides are known as DNA chips. It is used to detect potato viruses, cucurbitinfecting tobamoviruses, and grapevine viruses (Bystricka et  al. 2003; Lee et  al.

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2003; Nicolaisen 2011). It is not quite the same as the above method in this point of view because it gives expression estimations of characterized genes of the set (Eshaque and Dixon 2006). Within a small surface area, thousands of DNA probes are displayed on a matrix that consists of glass chip or nylon filters in this technology. Sample position is called spot on the chip (Robinson et al. 2000). On the support matrix, these probes are immobilized, and focused cDNAs are useful as a hybridization chip. The Quantification encircled cDNA quantification is quantified using radio-labeled probes only after that signal is generated by hybridizing the probe to the focused mRNA that the specific software can identify and integrate. The Keen Software gives gene expression trend for every natural living sample (Russo et al. 2003). The microarray can detect a very large range of fungal cell. In the microarray techniques, large-scale DNA sequencing is not used. Even though this method can detect any changes in gene expression, noteworthy issues are noted. Initially, microarray required a lot of mRNA.  Besides, this investigation is constrained by the expense and right to use (Singh and Kumar 2013). Because of the abundant error steps in microarray technique, it is minimized by the repetition of the experiments. Microarrays are referred to as critical testing because it requires physical cell trouble to gain accesses to its patterns of gene expression; it is remembered that false data can be generated by the mRNA degradation (Singh and Kumar 2013). This technique can detect bacteria, viruses, parasites, fungi, viroids, and phytoplasmas (Hadidi and Barba 2006). Postnikova and Nemchinov (2012) used microarray-­based analysis for the comparative study of the various viruses in Arabidopsis. Leborgne and Bouhidel (2014) studied plant-microbe interaction using microarray. Osmani et al. (2019) used microarray analysis to detect responses of various viruses of potato.

6.4.12 Macroarray It is also known as the hybridization of the DNA array or the plot of the reverse dot. It utilizes the feasibility of DNA amplification while radioisotopes are not required (Singh and Kumar 2013). In a growing number of labs around the world, macroarray is a quick molecular technique for the diagnostic of greenhouse plants (Le Floch et al. 2007; Lievens et al. 2003), ginseng (Punja et al. 2007), and potatoes (Fessehaie et al. 2003). It’s working according to concurrent amplification of the linked species by the PCR. Also, in one hybridization reaction, it simultaneously analyzes several amplified sequence. It is a technique that is more sensitive and sophisticated than other PCR (Taoufik et al. 2004). In this evaluation amplification of PCR is joined with hybridization that builds affectability up to thousand folds or higher than PCR only technique, and it has a quick rotation time 1–2 days in contrast with radioactive culture techniques that involve 2 months for their conclusion (Taoufik et al. 2004). In this technique, the inward probe is considered to separate the variety. These probes are attached to the hold of the nylon membrane. By ultraviolet cross-linking, oligos are eternally bound to the membrane. The amplified PCR products are firstly hybridized and then spotted on the strips where species-specific interaction takes place (Tsui et  al. 2011; Leinberger et  al. 2005). To identify the species level of

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Mycobacterium, the combination of the PCR and microarray technique is used (Leinberger et  al. 2005). It is also used to detect Alternaria alternata, Fusarium solani, Candida albicans, Aspergillus fumigates, and Cladosporium herbarum (Sato et al. 2010) and identification of fungal as well as oomycete of the pathogen that causes the illness in solanaceous plants (Zhang et al. 2008).

6.4.13 Loop-Mediated Isothermal Amplification (LAMP) LAMP has a vigorous and new approach for amplifying nucleic acid as a substitute for PCR. LAMP amplified specific nucleic acid with high specificity under the isothermal situation. It never requires PCR to produce changes in temperature but requires a single Tm for amplification of DNA molecule (Tsui et al. 2011). This technique is also based on auto-cycling and strand dislocations. LAMP utilizes polymerase of Bst DNA and two sets of internal and external primers. This reaction works at 650C for an hour while being put on either a dry or water bath, and after that, SYBR Green can be used for the detection of the amplified product. The end product of the LAMP has numerous reverse repeat with several loops which show cauliflower-like structure. LAMP is ten times greater exact and accurate than standard PCR (Ren et al. 2009). In LAMP, thermal changes are not needed; as compared with PCR, LAMP reaction requires only one tube (Fakruddin 2011). The sensitivity of LAMP reaction is affected by various factors, i.e., utilization of the DNA polymerase. This is significant for LAMP effectiveness. For recognition and diagnosis, LAMP is useful but it cannot be utilized for cloning purposes. While, the major disadvantage of LAM is, it cannot used for the direct assessment different dyes, for example Mn2+ (dye), SYBR Green dye, hydroxyl naphthol blue dye etc. that cannot be distinguished among the required specific amplified product size and non specific product size, So, lead to false positives result. It can be resolved due to the utilization of molecular beacons (MBs) by producing the fluorescence signals while it combines with specific DNA sequences. Therefore, MBs can detect the amplified product. The LAMP finds a suitable situation for MBs (25–45 bp beacon length, 60–65 °C reaction temperature, and 0.6–1 pmol/μL beacon concentration) for the evaluation technique. An original MB-LAMP-based method has proven direct identification of the LAMP product. MBs are the nucleic acid fluorescent sample with hairpin structure. The structure of the hairpin left the fluorescence as quencher that is near to a fluorophore (Liu et al. 2017). LAMP detects Ascochyta rabiei fungi that cause Ascochyta blight disease in chickpeas. The contrast of standard PCR and LAMP not only reveals superior accuracy, sensitivity, and specificity to detect A. rabiei but also utilizes simple apparatus and takes less time to operate (Chen et  al. 2016). LAMP was successfully used to identify Paracoccidioides brasiliensis, a thermal-reliant dimorphic fungus (Endo et al. 2004). This method also detects the pathogenic fungus, i.e., Ochroconis gallopava (Tsui et al. 2011). The use of lamp technology has also efficiently diagnosed Penicillium marneffei (Sun et al. 2010). Recently, LAMP is used to identify Ophiostoma clavatum, main blue stain fungus (Villari et al. 2013), Colletotrichum gloeosporioides (Wang et al. 2017), and whitefly Bemisia tabaci (Blaser et al. 2018).

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6.4.14 Sequencing of the Next Generation Based on RNA-Seq RNA sequencing is a recently developed technique for deep sequencing. A huge populace of RNA are generally transformed into a library of cDNA with adapters that bind to single or both ends. After that, every sequence having with or without amplification is sequenced for obtaining minute sequence from one end as in single-­ end sequencing or both ends as in pair-end sequencing in a high-throughput way. Based on DNA, sequencing tools can be used for reads which are commonly up to  30,400  bp. Prepared library to observe how strongly the results of the RNA sequencing unveil that most of the unique RNA transcripts are identified in the step of preparation of the library. To build up an RNA sequence library, it is necessary to fragment RNA or DNA moreover to permit processing by sequencing of the next generation. In the real-time reaction, mRNA can be prepared using either oligo or random primers. The benefit for the utilization of oligonucleotide is the significant production of polyadenylated mRNA proportion of cDNA. Therefore most of the acquired sequence can be insightful (Mortazavi et al. 2008). The three very generally RNA-Seq technologies of next generation are SOLiD and Ion Torrent, which are produced by Life Technologies, and HiSeq by Illumina (Dawei and Peng 2014). After that sequencing, we found the maximum reads that are either aligned with reference genome whose sequences are known or constructed with de novo sequence without genomics sequence to develop a transcriptional map consisting of both expression level of every gene and transcription structure. Although RNA sequencing data obtained  that can be  used for  alignment with the referred genome data, Annotator and Trinity assembler that assemble the RNA sequencing data without reference genome data using the assemble of adjacent identification of shorts reads. These methods enable new transcripts to be discovered and numerical transcript to be detected fairly. They are allowing more efficient use of the RNA sequencing to detect transcripts and classify the transcriptome in a nonmodel organism (GrabHerr et  al. 2011). The Magnaporthe oryzae fungus is detected using this technology, which induces rice blast disease (Soanes et al. 2012). Verticillium dahliae fungus in tomatoes that induces vascular wilt disease is also identified using this technique (de Jonge et al. 2012). RNA sequencing would be used to detect pathogens in plants. The prospective suitability of mRNA sequencing data to recognize nucleotide divergences can disclose fungal pathogenicity genes of the plant in their protein-coding transcriptome that is mutant. The technique allows us to diagnose plant disease using RNA measurements (Metzker 2009).

6.4.15 Lateral Flow Microarrays Nucleic acid is rapidly detected using lateral flow microarrays (LFM) based on hybridization technique with colorimetric signals that can be easily visualized (Carter and Cary 2007). LFM based on lateral flow nitrocellulose membrane chromatography, hybridized in very less time, have detection limits and might decrease the requirement for high-price lab tools. Skill is dependent for accessibility of

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useful and reliable biomarkers of host and pathogen revealed by transcriptomics perspective (Martinelli et al. 2012a, 2013a). While we can use metabolomics for the detection of primary and secondary metabolites; it can be utilized as a biochemical marker for a variety of pathogenic diseases (Rizzini et al. 2010; Tosetti et al. 2012; Martinelli et al. 2012b, 2013b, 2014; Ibanez et al. 2014). Early pathogenic infections like Huanglongbing disease in citrus can be identified by an included omics approach (Dandekar et  al. 2010). More highly synergistic proteins are necessary markers for plant health status, i.e., heat shock protein (HSP) or dehydrins, upregulated by various ecological ways (Natali et al. 2007).

6.5

Remote Sensing (RS)-Based Diagnostics

Spectroscopy is one of the main useful RS methods, including sensors such as VIS, NIR, SWIR, and imaging or nonimaging. Due to their possibility as a functioning instrument, elasticity, efficacy, and cost-effectiveness, these tools hold exciting promise for crop disease monitoring. Below are discussed the most applicable and recent developments in spectroscopy depending on techniques.

6.5.1 Nonimaging Spectroscopy It is based on the natural things of leaf pigments, chemical factor, properties, and structural characteristics (Jacquemoud and Ustin 2001). Laboratory or field-­collected leaf spectra determined spectral area of visibility for identification of diseases, i.e., leaf gall disease in sugarcane through remote sensing (Purcell et al. 2009), powdery mildew disease in wheat (Graeff et al. 2006), curl mite (Stilwell et al. 2013), yellow leaf virus in sugarcane (Grisham et al. 2010), also yellow rust in wheat during winter (Zhang et al. 2014), and grapevine viruses in grapes (Naidu et al. 2009). Yuan et al. (2014) experimented with the separation of winter contamination from pathogens, insects such as wheat aphids, and virus, i.e., yellow rust and powdery mildew. Methods for early identification of disease are of faithful interest (Malthus and Madeira 1993; Delalieux et al. 2007; Rumpf et al. 2010), while their actual use is incoherent across crops for crop management. Studies available are crop definite, and results cannot be comprehensive with comparable accuracy to other crops and places. When  Huang et al. (2012) compared both, firstly canopy scale detection of leaf and severity determination of rice leaf folder disease, the best concurrence of recognition rates using VIS and NIR reflection by linear regression method and the NIR plateau has a very high negative correlation (737–1000 nm) and severity of infestation. Many authors are working with radiometry to determine the harshness of the damage of crop (Nutter 1989). Yang et  al. (2007) reported that rice plants are infested with brown plant hopper and leaf folder. Mirik et al. (2006) studied spoil from green bugs to winter wheat, Chen et al. (2008) Accessed loss of cotton from Verticillium wilt and studied leafhopper disease from Prabhakar et al. (2011). Also utilized for fruit value evaluation was spectroscopy, often connected with additional

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resources, i.e., e-nose data; booming integration of remote sensing depends on the way with VOC analysis (Costa et al. 2007).

6.5.2 Imaging Spectroscopy Hyperspectral imaging tools have recently been integrated to evaluate and observe plant illness. Lab experiments detect various diseases, i.e., head blight disease in wheat, a fungal disease with Fusarium (Bauriegel et al. 2011), sugar beet disease (Mahlein et al. 2012) on leaves, rust, and powdery mildew (Mahlein et al. 2013). Diverse infections and its stage of maturity are of particular interest for effective intervention (Mahlein et al. 2012). This report utilized a wide range of statistical instruments for image investigation, such as linear regression, principal component analysis (PCA), spectral angle mapper (SAM), and support vector machine (SVM) categorization with elevated accuracy of detection of disease. However, these trials concentrated on one or a few plants with little probability of generalization. On the basis of field survey of wheat plant yellow rust disease (Bravo et al.) and attempts to distinguished among wheat disease and abiotic stress (Moshou et  al. 2004), Reynolds et  al. (2012) and Huang et  al. (2007) used the hyperspectral field and aerial information for evaluating the seriousness of Rhizoctonia crown and root rot disease in sugar beet and yellow wheat rust, respectively. Airborne hyperspectral data is best suited for farm and regional-scale remote sensing (RS) applications.

6.6

Protein-Based Diagnostics

6.6.1 MALDI-TOF MS Bacterial product isolates were subcultured on LB agar media (Thermo Fisher Scientific, UK) and incubated at 37 °C for a 24–48 h and recognized with a Bruker MALDI biotyper system (microflex LT, Bruker) as directed by the manufacturer. The calibration of the mass spectrometer was performed by an automatic calibration operation with Bruker bacterial test standard (BTS), which is a modification of E. coli BH5α, spiked using two extra enzymes to allow calibration with 4–17 kDa mass ranges. After 6x40 laser shots have been implemented, a sum spectrum is automatically acquired from separate locations on BTS control. The minimum amount of peaks reverted to seven after the calibration phase (Fig. 6.2). Using a sterile toothpick, an individual colony from a new culture of each isolate was selected and smeared on the specified places on normal MALDI target plate, and the drying plates were put on RT (25 °C) for 5 min after loading the sample. 1 μl HCCA matrix (saturated solution of α-cyano-40hydroxycinnamic acid in 50% acetonitrile and 2.5% trifluoroacetic acid) was put on the top of a spot not more than 10 min of drying the samples. Before loading plate into a mass spectrometer, sample was air-dried again for 5 min. Every bacterial colony has been screened in duplicate. MALDI Biotyper Real-time Classification (MBT-RTC) software (Bruker) acquired data set. It compares unknown peak from the reference database (MBT

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Fig. 6.2  MALDI-TOF method for the identification of the microbes from the infected plant

Compass 4.1, Bruker) as well as used statistical algorithm to produce a log score ranging from 0.000 to 3.000. The classification score was considered to be suitable for species-level recognition  (>=2.000 confident species identification), although recognition of the genus level (1.700–1.999 confident genus identification), below 50%) that exhibit the critical level of 1.5 ppm of available zinc (Katyal et  al. 1994). The plant alone cannot absorb Zn from the soil, and hence farmers apply a huge amount of zinc sulfate (ZnSO4) as an external fertilizer application. However, external fertilizer application also does not work well because the plant utilizes a very low percentage (1–4%) of the total available Zn and 75% of the applied Zn is transformed into different mineral fractions (Goteti et al. 2013). Two core mechanisms are applied to fix Zn: one is cation exchange, which mostly operates in acidic soils, and the other operates in alkaline conditions, where fixation

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occurs using chemisorption (chemisorption of zinc on calcium carbonate [CaCO3] forms a solid-solution of Zn by complexation of organic ligands; Alloway 2008). Microbe-based solubilization of Zn plays a significant role in the soil, and major bacterial inoculants that fix Zn are Bacillus subtilis, Thiobacillus thiooxidans, and Saccharomyces sp., Burkholderia sp., and Acinetobacter sp., and these microbial inoculants are used as biofertilizers (Azooz and Ahmad 2013; Vaid et  al. 2014). Mahdi et al. (2010) reported that Zn-solubilizing microbes are mostly applied in soils where native Zn is higher or in conjunction with insoluble cheaper zinc compounds like zinc oxide (ZnO), zinc carbonate (ZnCO3), and zinc sulfide (ZnS) instead of costly zinc sulfate  (ZnSO4)). Kamran et  al. (2017) reported that Zn-solubilizing microbes include Rhizobium sp. (LHRW1), while Enterobacter cloacae (PBS 2) improved Zn uptake in wheat plants and enhanced the root and shoot biomass. Dinesh et  al. (2018) concluded that Zn-solubilizing Bacillus megaterium ZnSB2 strain played a significant role in Zn dissolution in soil, and it would allow reducing the utilization of inorganic Zn application rates. Gontia-Mishra et al. (2017) assessed that Zn-solubilizing bacteria such as Pseudomonas aeruginosa, Ralstonia picketti, Burkholderia cepacia, and Klebsiella pneumoniae improve the growth of rice seedlings and these bacteria could be used as Zn mobilizers for profitable farming.

7.9

Microbes Play a Role in Biofertilization

In the past several decades, chemical fertilizers have been applied as a source of major plant nutrients such as nitrogen, phosphorus, and potassium. These fertilizers improved the crop production but enhanced the farming cost and also polluted the natural resources that increased the environmental risks (Gong et al. 2011; Machado et al. 2017; Mullin et al. 2010; Vitousek et al. 2009). The plants themselves cannot utilize the insoluble forms of P and N2. Therefore, plant growth-promoting microbes that can fix N2 and solubilize the P are used as biofertilizers (Zahir et  al. 2004; Schütz et al. 2018; Zaidi and Khan 2006; Alori et al. 2017). These microbe-based biofertilizers are environment-friendly and less expensive as compared to the chemical fertilizers. These biofertilizers improve the nutrient accumulation in the plant root by a different mechanism, such as mobilization, solubilization, and absorption, and enhance P uptake and N2-fixation. Moreover, biofertilizers also play a significant role in the uptake of micronutrients like Fe, Cu, Zn, B, Mn, Co, and Mo (Bargaz et al. 2018). Several reports also concluded that mixed inoculation of N2-fixing and phosphate-solubilizing bacteria had provided more balanced nutrition to different agriculture crops such as sorghum, barley, black gram, soybean, and wheat (Abd-­ Alla et al. 2001; Alagawadi and Gaur 1992; Galal 2003; Tanwar et al. 2003) Rhizobium is one of the prominent diazotrophs that is mostly used as a biofertilizer alone in India, but the use of Rhizobium in combination with phosphate-­ solubilizing bacteria (PSB) needs to be explored more extensively. Nevertheless, application of combined microbe inoculum to enhance the soil fertility is getting the attention of researchers (Basak and Biswas 2010; Dash et al. 2018; He et al. 2019; Kant et  al. 2016; Sharma et  al. 2019). Recent findings specified that combined

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inoculation of plant growth-promoting rhizobacteria (PGPR) in arable soils enhanced the crop yield significantly (Harish et al. 2009a; Harish et al. 2009b). The PGPR strains Pseudomonas alcaligenes PsA15, Bacillus polymyxa BcP26, and Mycobacterium phlei MbP18 had positive impact on maize plant health and the uptake of N, P, and K in nutrient-deficient Calcisol soils (Egamberdiyeva 2007; Verma et  al. 2017a). These PGPRs have a strong ability to produce growth-­ promoting phytohormones and play a significant role in phosphate mobilization, production of siderophore and antibiotics, inhibition of plant ethylene synthesis, and induction of plant systemic resistances to pathogens that helps to enhance the crop yield (Cakmakçi et al. 2006; Han and Lee 2006; Kohler et al. 2006; Turan et al. 2005; Zahir et al. 2004; Zaidi and Khan 2006). PGP endophytes also play a significant role in plant growth regulation (Suman et al. 2016b). Rhizobium, Azotobacter, Azospirillum, Cyanobacteria, Azolla, Phosphate, and potassium-solubilizing microorganisms are the most applied microorganisms that are considered as beneficial for sustainable agriculture and used as biofertilizers. Silicate-solubilizing bacteria also help to promote plant growth and are available as liquid biofertilizers (Parewa et al. 2014; Suman et al. 2016a; Verma et al. 2014a; Zhang and Kong 2014). Microbes and their beneficial association with crop plants are listed in Table 7.3.

7.10 Economic Development in Agriculture Microbe-based biofertilizer development is accepted as a relevant approach to increase food production (Schütz et al. 2018). Global population pressure as well as climate change have become serious constraints for the economic growth of several countries and food security (Cole et al. 2018). Fundamentally, to improve the soil and plant health, two major strategies need to be followed: (1) extensive application of microbe-based biofertilizer, and (2) the manipulation of naturally existing microbial populations (Patil and Solanki 2016; Schütz et al. 2018). Mostly, PGPRs that are grown as either saprophytic or endophytic symbionts are protagonists of applied microbial biotechnology in agriculture (Backer et al. 2018). Especially, microbial formulation, quality control, and modes of application of microbial inoculants are getting the attention of researchers (Singh et al. 2014; Velivelli et al. 2014). Several mechanisms underlying the plant–microbe interactions in the rhizosphere and plant still need to be explored in depth. Researchers are facing difficulties, mostly regarding how to utilize the large microbial structure, especially unculturable microbes, to boost the soil and plant health. Secondary, a plethora of culture-independent molecular techniques is becoming accessible and is presently being applied either to interpret the hidden networks of microorganisms inhabiting soil and rhizosphere microenvironments or to outline the molecular bases of the plant–microbiome interactions (Patil and Solanki 2016). Multitrophic factors, including nutrient deficits, salt, low water, air contamination, diseases, and pests, cause negative impacts on the functionality/productivity of agricultural products and plant systems (Fig. 7.2). Agriculture plays an indispensable role in the Indian economy, and biofertilizers are essential to improve crop yield in an eco-friendly manner (Kesavan and

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Table 7.3  Microbial linkage promoting various types of growth in plants to improve crop yield S. No. 1.

Types of growth promotion in plants Growth enhancement of canola and lettuce

Microbial inoculants Rhizobium leguminosarum

2.

Early developments of canola seedlings

Pseudomonas putida G 12-2

3.

Growth enhancement of wheat and maize plants

Azospirillum brasilense and Azospirillum irakense strains

4.

Growth enhancement of pearl millet

Pseudomonas fluorescens strain

5.

Growth stimulation of tomato plant

Pseudomonas putida strain

6.

Growth and productivity enhancement of canola

Azotobacter and Azospirillum strains

7.

Enhanced uptake of N, P, and K by maize crop in nutrient-deficient Calcisol soil Growth and yield enhancement of chick pea (Cicer arietinum)

Pseudomonas alcaligenes PsA15; Bacillus polymyxa BcP26; Mycobacterium phlei MbP18 Pseudomonas, Azotobacter, and Azospirillum strains

Improvement in the yield and phosphorus uptake in wheat Improvement in seed germination, seedling growth, and yield of maize

R. leguminosarum (Thal-8/ SK8); Pseudomonas sp. strain 54RB P. putida strains R-168 and DSM-291; P. fluorescens strains R-98 and DSM-50090; A. brasilense DSM-1691; Azospirillum lipoferum DSM-1690 P. putida strain R-168

8.

9.

10.

11.

Improvement in seed germination, growth parameters of maize seedling in greenhouse, and also grain yield of field-grown maize

References García-Fraile et al. (2012); Noel et al. (1996); Singh (2013) Glick et al. (1997); Hwang et al. (2011); Zhang et al. (2015) Couillerot et al. (2013); Dobbelaere et al. (2002); Fukami et al. (2016) Fukami et al. (2016); Karnwal (2012); Raj et al. (2003) Gravel et al. (2007); Mariutto et al. (2011); Pastor et al. (2014) Naderifar and Daneshian (2012); Naseri et al. (2013); Yasari and Patwardhan (2007) Egamberdiyeva (2007); Saharan and Nehra (2011); Shrivastava and Kumar (2015) Joseph et al. (2012); Rokhzadi et al. (2008); Rokhzadi and Toashih (2011) Afzal and Bano (2008); Mehboob et al. (2012); Shaikh et al. (2016) Gholami et al. (2009); Karunakaran et al. (2013); Shen et al. (2010)

Gholami et al. (2009); Noumavo et al. (2013); Singh et al. (2011)

(continued)

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Table 7.3 (continued) S. No. 12.

13.

Types of growth promotion in plants Increase in growth, leaf nutrient contents, and yield of banana cv. Virupakshi (Musa spp. AAB) plants Improvement in seed germination, growth parameters of wheat seedling in pots, and also grain yield of field-grown wheat

Microbial inoculants P. fluorescens strain R-93; P. fluorescens DSM 50090; P. putida DSM291; A. lipoferum DSM 1691; A. brasilense SM 1690; P. fluorescens strains CHA0 and Pf1 Bacillus amyloliquefaciens IARI-HHS2-30

References Kavino et al. (2010); Patil (2013); Selvarajan and Balasubramanian (2014)

Verma (2013, 2015, 2016); Verma et al. (2014a, b, 2016)

Fig. 7.2  Microbes and their role in the intensification of sustainable agriculture

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Swaminathan 2008). Out of India’s total geographical area (329 million hectares), about 114 million hectares are under farming (Raghuwanshi 2012). To gain better yield, farmers vaccinate the soil with fertilizers. These fertilizers belong to two classes. They are either inorganic chemical or organic biofertilizers. Increasingly high inputs of chemical fertilizers during the last 150 years have not only negatively influenced the fertility of the soil but also polluted the water sources. Soil fertility degraded significantly, and polluted resources have also posed severe health and environmental hazards (Schütz et al. 2018). In contrast, microbe-based biofertilizers not only give a better yield, but are also harmless to the ecosystem (Patil and Solanki 2016). Biofertilizer-based organic farming methods would help solve these concerns and boost the ecosystem (Shukla et  al. 2016). In the present time, organic biofertilizer market has reached around US$ 30 billion globally and with an excellent growth rate (8%). Approximately, 22 million hectares of agricultural land is now cultivated organically by the use of microbe-based fertilizers. However, organic farming represents less than 1% of the world’s conventional agricultural production and about 9% of the total agricultural area (Verma et al. 2014b). To have an environmentally safe technology, microbial product-based agriculture system needs to be used efficiently.

7.11 M  icrobial Engineering Gets Better Agriculture and Human Health A microbial structure is composed of and influenced by host location and environmental factors that generate undesirable phenotypes in the hosts. The disturbance of microbiome negatively affects the associated ecosystems that cause diseases and disorders in the host. Microbiome engineering can be used to modify or restore the microbial community to improve the plant and human health. Foo et al. (2017) discussed the vitality of microbiome engineering toward agriculture prospects and human health. Plant microbiome can be planned with known microbial inoculants with desired functions to get significant production in an eco-friendly manner. Santhanam et al. (2015) reported an example of artificially developed microbiome by using five root-associated bacteria that significantly reduced the sudden-wilt disease in Nicotiana attenuata. Additionally, Glick (2012) assessed co-inoculation of rhizobacteria had shown higher growth and yield in various crops as compared to the single microbes. Soil microbiome engineering is usually flourished by hiring different agricultural practices such as intercropping, crop rotation, and tillage (Fageria 2012; Solanki et al. 2017, 2019). Application of green organic manure, farmyard manure, is also one of the important agriculture practices that enhance the soil microbiomes significantly (Chaparro et  al. 2012; Abebe and Deressa 2017). All these agricultural practices targeted to modify the soil microbial diversity, mineral cycles, and biological activity, and these significantly helps to reduce the off-farm inputs, for example, chemical fertilizers and herbicides.

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In the present scenario, microbial engineering is most extensively utilized to modify the human microbiome to improve immunity and disease resistance. Advanced biotechnological tools help to manipulate human microbiome to treat diseases such as diabetes and cancer; modified microbiota influence the host metabolism that helps to regulate diseases (Grice and Segre 2012). Meat industry badly suffered from antibiotic-resistant bacteria, and it has become the most common problem for livestock farming. Thus, microbiome alteration of livestock by using feed enzymes, prebiotics, and probiotics is a suitable alternative as compared to the overdose of antibiotics that also negatively affect human health. To promote gut health in swine and poultry, feed enzymes like phytase, amylase, non-starch polysaccharide (NSP)-degrading enzymes (e.g., xylanase, β-glucanase, and β-mannanase), proteases, and lysozyme are used that enhance the substrate digestion, improve the production of prebiotics from dietary NSPs, and reduce the antinutritive factors (Archna et al. 2015; Kiarie et al. 2013; Verma et al. 2015b).

7.12 Conclusion and Future Prospects During the past several decades, microbial research has made significant progress in sustainable agriculture. Subsequently, advanced microbiological tools offer to use microbial engineering to alter microbiota of human and plant to improve health and increase production. However, plant microbiome and different environmental stress need to be explored to reveal a unique signaling network among microbes that help the plant to survive. Characterization of these signaling molecules can help to design advanced biotechnological strategies that unlock the plant adaptation mechanisms. Similarly, soil health can be flourished by using the crosstalk of soil microbes. Moreover, different microbial tools and agriculture technologies are being established, providing deeper insights into the plant/soil microbiomes, and these tools widely help to accelerate the microbial engineering efforts. With nonstop hard work in understanding and manipulating microbes, the microbial link will be a mainstream approach for refining human health and agriculture output. Acknowledgments  We are grateful to the Department of Microbiology, Akal College of Basic Science, Eternal University, Himachal Pradesh, and Department of Biotechnology (DBT), Ministry of Science and Technology, for providing financial support to carry out field studies.

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8

Wheat Microbiome: Present Status and Future Perspective Sunita Mahapatra, Pravallikasree Rayanoothala, Manoj Kumar Solanki, and Srikanta Das

Abstract

Wheat microbiome harbors a diverse array of microbial communities and play a vital role in maintaining wheat physiology as well assist in offering protection from biotic and abiotic stresses. Several research findings indicated that wheat microbiome encompasses predominantly fungi, bacteria, viruses, actinomycetes, cyanobacteria, protozoa, archaea, etc. which performed myriads of advantageous activities including bio-management of crop pathogens, abiotic stress amelioration, as well as plant growth promotion under adverse conditions. In this chapter, attempts have been made to provide comprehensive and up-to-date insights on wheat microbiome research with major emphasis on emerging microbiome-­ based sustainable solutions for profitable and quality wheat production under every changing climate. Keywords

Abiotic stress · Bio-antagonist · Microbiome · PGPR · Wheat

8.1

Introduction

Wheat (Triticum aestivum) is the largest cultivated crop in the world occupying an area of 222.35 million hectares with an estimated production of 753.89 million tons in 2016–2017 (Jasrotia et al. 2018). It is a staple food in more than 40 countries and S. Mahapatra (*) · P. Rayanoothala · S. Das Department of Plant Pathology, Bidhan Chandra Krishi Viswavidyalaya, Mohanpur, Nadia, West Bengal, India M. K. Solanki Department of Food Quality & Safety, Institute for Post-harvest and Food Sciences, The Volcani Center, Agricultural Research Organization, Rishon LeZion, Israel © Springer Nature Singapore Pte Ltd. 2020 M. K. Solanki et al. (eds.), Phytobiomes: Current Insights and Future Vistas, https://doi.org/10.1007/978-981-15-3151-4_8

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finds a significant share of about 35% in the consumption basket of millions across the world. It is estimated that global population depends on wheat for 85% and 82%, respectively, for calories and protein (Chaves et al. 2013). Moreover, wheat meets up 21% of the world’s food demand and is grown on 200 M ha of farmland globally (Tsvetanov et al. 2016). By 2050, the world will have the challenge to meet the food demand of an estimated population of 9.6 billions. Feeding for growing population at the era of climate change requires the use of optimized, reliable and existing resources which have less impact on the environment (Busby et al. 2017). Now research topics mainly highlighted on the issue of not only quantity but also quality of food product with minimal uses of existing earth resources. Under developing countries like India, which has self-sufficiency in wheat production, there is a need to give emphasis on quality wheat production by understanding plant microbiome and its interactions with environment and stress regimes. Moreover, the future global climate scenarios predicted an increase in the occurrence of exceptionally hot days, together with an increase in average global temperatures and its implications on global food production. Asseng et  al. (2015) reported that the global wheat production is influenced by the increase of temperature and becomes more variable over space and time. In Indian perspective, temperature changes in the last 30  years had a bigger impact on national wheat production, where over 90% of wheat is irrigated (Singh and Mustard 2012), than changes in precipitation (Lobell et al. 2011). One of the most important cropping patterns in South Asia is rice-wheat cropping system, facing immense pressure because of heat stress and degraded soil health due to high cropping intensity and tillage for growing rice and over-exploitation of the natural resources (Joshi et al. 2007). The most affected locations of South Asia are eastern Gangetic plains, central and peninsular India and Bangladesh. Besides, a substantial proportion of cultivated land under wheat in South Asia is salt affected. The salt-affected land under wheat in India is 4.5 m ha, whereas 6.0 m ha in Pakistan amongst the other South Asian countries (Singh and Chatrath 2001). Although soil reclamation and provision of proper drainage may be more effective solution, it does not seem possible in the near future due to huge acreage affected by salt. Another constraint is deficiency of macro-nutrients like zinc, sulphur, iron, manganese and boron which are being observed in some pockets of northern India, Bangladesh and Nepal due to imbalanced fertilization, overmining of essential plant nutrients and burning of crop residues (Chatrath 2004). Water is also becoming scarce as the water table is going down due to overmining of groundwater in intensive rice-wheat cultivation and comparatively less water recharge from monsoon rains. Amongst the biotic stresses, rusts continue to be the major threat (Khan et al. 2017; Savadi et al. 2018; Singh et al. 2006; Kumar et al. 2019; Kashyap et al. 2019). Out of three rusts prevalent in Indian subcontinent, leaf rust is the major disease which affects almost whole of India, parts of Bangladesh and Nepal. Spot blotch caused by Bipolaris sorokiniana (Sacc.) Shoem is also considered an important disease in the eastern part of South Asia (Joshi et al. 2007; Devi et al. 2018). In addition, other diseases, viz. Karnal bunt, powdery mildew and wheat blast also affect wheat crop to some extent (Singh 2017; Kashyap et  al. 2011, 2018, 2019;

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Nallathambi et al. 2019; Kumar et al. 2020). The use of microbiomes increases crop productivity, reduces the cost of cultivation and sustains the health of soil as well as environment. Use of microbiome in wheat cultivation has the ability to change the entire scenario of the current agricultural and food security. The plant microbiome is a key determinant of plant health and productivity and has received substantial attention in recent years. There is an expanded version of the tree of life dominated by bacterial diversification due to their ability to perform lateral gene transfer across disparate phylogenetic groups (Mcdonald and Currie 2017; Hug et  al. 2016). Recent advance researches in high-throughput sequencing technique and the increasing number of microbial culture libraries, they can quickly proliferate and have high mutation rates (Kibota and Lynch 1996; Boe et  al. 2000; Denamur and Matic 2006). Individual microbes of the same species could potentially bear different genetic endowments and thus functional characteristics (Sergaki et al. 2018). Amplicon sequencing has been invaluable in determining general patterns of microbial diversity within the plant microbiome (Bulgarelli et  al. 2012; Lundberg et  al. 2012; Peiffer et  al. 2013; Tkacz et al. 2015). However, use of microbiome on wheat is very limited. Most of the previous studies mostly based on identifying microbes in the root’s rhizosphere (Hartmann et al. 2014; Mahoney et al. 2017; Ofek et al. 2013; Yin et al. 2017) and limited research work is  focused on aboveground organs (Granzow et  al. 2017; Huang et al. 2016; Karlsson et al. 2017). To our knowledge, till date no detailed published works are available on entire wheat microbiome, including both above- and belowground plant organs, mode of actions, how they work under stress conditions and what are the easy and fast way of identification with high-throughput sequencing techniques. Here we classify the microbiome in a detailed way and also use fullness of those microbiomes especially for wheat crop. But still microbial communities were dependent on type of plant organ, growth stages of the plant, environmental conditions, acceptability amongst the farmers and community composition, etc.  and therefore need to be  checked before their successful intervention and execution.

8.2

Plant Microbiome: Concept and Definitions

Microbes are associated with majority of living species and are omnipresent in nature. However, majority of them are noticed in harsh environments. The microbial diversity consists of various types of microbes such as archaea, bacteria, cyanobacteria, fungi and protozoa (Vessey 2003; Verma and Suman 2018). The plant microbiomes include rhizospheric, endophytic and epiphytic microbes which help in plant growth and in adaptation even in extreme environments. In our planet, researchers have recorded the presence of microbiomes amongst 1.7 million living species and noticed that 1–10% bacterial species are present amongst 5000 species of prokaryotes (Federhen 2014; Moore 2014). The microbiomes are useful in industry and

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medical processes too in addition to agriculture, and they act as abundant reservoirs of bioresources. Thus in keeping good soil health, enhancing productivity and improving the growth of plants, these plant microbiomes play vital role and are found helpful in providing a sustainable biosphere. The following definitions are found for plant microbiome in literature. 1. Bulgarelli and Schlaeppi (2015) have defined microbiota or microbiome as a set of genomes of the microorganisms in some habitat. 2. Several researchers have defined that microbial communities are the ones associated with any plant that can live, thrive and interact with various tissues such as roots, shoots, leaves, flowers and seeds (Turner et al. 2013; Haney and Ausubel 2015; Mueller and Sachs 2015; Haney et al. 2015; Nelson 2018). It is also found in literature that microbiome includes all the microbes of a community.

8.3

Wheat Microbiomes: Concept and Types

The wheat microbiome is mainly composed of various kinds of organisms such as archaea, protozoa, bacteria, fungi and virus (Mueller and Sachs 2015). Research done on the microorganisms so far found that they are present in healthy crops, and their findings are limited to species of wild Triticum and of wheat (Marshall et al. 1999). It is a well known fact that nematodes, ants, moles and several fungi and bacteria take common shelter in soil. They play an essential role in protecting the plant from potential plant pathogens and also in improving plant growth, health, and production (Berg et  al. 2014; Haney et  al. 2015). There is a closer association between plants and microbial communities and normally found at phyllosphere (above the ground), in rhizosphere (below the ground especially on roots and surrounding area of roots) and in endophytes (inside the root intercellular spaces) (Hirsch and Mauchline 2014). Relationship of plants with microbes is beneficial in improving disease resistance, in increasing stress tolerance levels and also in nutrient uptake. It is not always beneficial; rather, sometimes interactions of plants with microbes may be harmful too. This is dependent on kinds of bacteria involved, their characteristics and finally the ways of interactions. Mainly, the interactions between plants and microbes are classified as rhizospheric, endophytic and epiphytic (as shown in Fig.  8.1). Wheat plants interact mostly with either common microbes or niche-specific microbes (Fig. 8.2). Common microbes are Arthrobacter nicotianae, Bacillus amyloliquefaciens, B. sphaericus, B. subtilis, Paenibacillus amylolyticus, P. polymyxa, Micrococcus luteus, Pseudomonas aeruginosa and P. azotoformans, and most predominant species were reported from various parts of the plant such as phyllosphere, rhizosphere and internal tissues (Bhattacharyya and Jha 2012; Verma  and Suman 2018). Further, the wheat bacterial microbiomes belong to different taxonomic positions of phyla, namely, Actinobacteria, Bacteroidetes, Firmicutes, Proteobacteria and Gemmatimonadetes (Verma and Suman 2018). Some novel microbiomes like acidophiles, alkaliphiles,

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Endophytic microbiome

Rhizospheric microbiome

Fig. 8.1  Assemblage of microbes in and around wheat plant

Significance of endophytic bacterial metabolites Plant defense activation Bacterial signal transaction Plant bacterial communication Nutrient mobilization

Plant cell

Bacterial cell

Secretion of bacterial metabolites due to plant interaction Fig. 8.2  Relative distribution amongst different microbes isolated from phyllospheric, endophytic and rhizospheric sample of wheat

halophiles, psychrophiles, thermophiles and xerophiles are also found in wheat (Narula et al. 2006). According to Verma and Suman (2018), bacterial microbiomes, viz. Actinobacteria (12%), Bacteroidetes (7%), Firmicutes (32) and Proteobacteria (49%), which occupy a major portion, and three classes of bacteria, namely,

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Alphaproteobacteria (6%), Betaproteobacteria (8%) and Gammaproteobacteria (35%) are present in wheat.

8.3.1 Endophytes Wilson (1995) and Brader et al. (2014) observed that the bacteria or fungi during their life cycle attack the plant tissues. This invasion causes infections in plant tissues which are not apparent to the naked eye. However, these infections do not cause any symptoms of disease. Endophytic microbiomes get into plants through wounds and root hairs to benefit plants by colonizing them and preventing effects of pathogenic organisms. They may systematically colonize the plants (Compant et al. 2010; Kushwaha et al. 2020a). Requisite chemicals are produced by them to prevent the growth of plant pathogenic competitor organisms. Bacterial endophytes help plants in their growth  (Kushwaha et  al. 2019, 2020b). Carroll (1988) has done research on endophyte associations and shown that they enhance the survival chances against fungal pathogens. The specific endophytic species are Achromobacter piechaudii, A. xylosoxidans, Delftia lacustris, D. acidovorans, Acinetobacter lwoffii, Ochrobactrum intermedium, Pantoea dispersa, P. eucalypti, Staphylococcus epidermis, Pseudomonas monteilii and Variovorax soli and Serratia (Liu et al. 2010; Hallmann et al. 1997). Carroll (1988) has observed that host benefits is a common phenomenon related with fungal endophytes. Endophytic fungi are used as genetic vectors and as abundant source of secondary metabolites (Fisher et al. 1986; Stierle et al. 1993; Strobel and Daisy 2003). Further they act as biological control agents (Clay 1989; Bacon 1990; Schardl et al. 1991; Dorworth and Callan 1996). Hence, biotechnological interest is shown very much on endophytic fungi (Murray et al. 1992). It is also studied that fungal endophytes cause water loss in leaves. Some kinds of fungal endophytes help plants to survive in drought conditions and extreme temperature climates (El-Daim et al. 2014; Naveed et al. 2014; Khalafallah and Abo-Ghalia 2008). Thus, focused research has been done on it in general and on grass endophytes in particular (Farooq et al. 2009). Direct antagonism of microbial pathogens is one way that endophytic bacterial strains fuel plant growth. As biocontrol agents, endophytes induce resistance in plants to disease-causing organisms and allow plant to be healthy (Pleban et  al. 1995). Figure  8.3 described the isolation of host-associated endophyte and their vital function. The anti-microbial property of endophytic microbes generates secondary metabolites, and thus they act against pathogenic microbes (Tan and Zou 2001). There are many bioactive compounds different from endophytes, and such compounds belong to classes like alkaloids, flavones, peptides, phenols, quinines, steroids and terpenoids (Yu et al. 2010).

8  Wheat Microbiome: Present Status and Future Perspective

Plant growth Crop yield Plant fitness

Genetic engineering Microbial fermentation

Biocontrol agents

Plant biotechnology chemical process

Isolation of endophytic bacteria and fungi

Inoculation of plant Enhanced nutrient uptake

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Bioactive compound

Phytohorm on

Plant Stress regulator

Antibiosis Sederophore production

Fig. 8.3  Schematic representation of isolation, purification and function of endophytes in host plant

8.3.2 Epiphytic Microbiomes Synergy between plant and bacteria is due to the presence of epiphytic microbes on phyllosphere. Microorganisms found on leaf surfaces are identified as extremophiles due to their capacity to survive even at high temperature (40–55 °C). Further they tolerate ultraviolet radiation during the day and even cool temperature (5–10 °C) during the night (Kushwaha et al. 2020b). The association between the microorganisms in the phyllosphere influences the plant growth in natural habitat and the productivity of agricultural and horticultural crops for human consumption. The aerial parts of plants are normally exposed to air and dust. This helps typical microbiomes to get attached to the surface. Hence, survival and proliferation of the phyllospheric microbiomes on leaves depend on the leaf diffuses or exudates. Amino acids, glucose, fructose and sucrose are some nutrient factors found in the leaf exudates. Hence, the plant growth is accomplished by the essential process like nitrogen fixation (Iniguez et al. 2004; Venieraki et al. 2011). In the phyllosphere of wheat, researchers have observed the presence of microbes, viz., Achromobacter, Corynebacterium, Agrobacterium, Haemophilus, Alcaligenes, Arthrobacter, Bacillus, Azotobacter, Enterobacter, Lysinibacillus, Micrococcus, Brevundimonas, Paenibacillus, Methylobacterium, Micromonospora, Pseudomonas, Micrococcus, Streptomyces, Stenotrophomonas, Pantoea and Psychrobacter (Sharma et al. 2011a, b; Verma et al. 2016).

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Plant growth development

Physiology and metabolism

Tolerance to biotic and abiotic factors

Phyllosphere microbiota

Ecosystem productivity and management Agronomic application

Plant protection against pathogens Production of bioactive compounds Nutrient absorption Plant defense activation

Fig. 8.4  Function of phyllosphere microbiota

Production of bioactive compounds, tolerance to biotic and abiotic stress, immune response, agronomic applications, nutrient acquisition, ecosystem productivity and management, physiology and metabolism, plant protection against pathogen are some of the benefits happen due to phyllosphere microbiota and responsible for improved plant growth (Roat and Saraf 2017) (Fig. 8.4).

8.3.3 Rhizospheric Microbiome The microbiomes in rhizosphere predominantly gained importance due to attraction of different types of root exudate substrates, and this zone is considered a hotspot for microbial survival and its diversity compared to other plant parts (Arkhipova et al. 2005; Kuzmina and Melentev 2003). The rhizospheric microbiomes also play a vital role in growth of the plant. They are closely attached between roots and soils and help the plants in nutrient uptake. However, rhizospheric microbiome is greatly affected by several factors like soil types, pH values, soil moisture and presence of micronutrients in soil etc. (Ahemad and Kibret 2014; Khalid et al. 2004). Rhizospheric microbes live in soil near roots, and due to gradient of root closeness they utilize metabolites from the surrounding roots as carbon and nitrogen sources and they inhabit spaces between cortical cells, they colonize rhizoplane and also they live in the specialized root structures like root nodules. Specific species of the rhizospheric are Pseudomonas extremorientalis, P. rhizosphaerae, Arthrobacter nicotinovorans, Azotobacter tropicalis, Bacillus atrophaeus, B. horikoshii, B. mojavensis, B. siamensis, B. thuringiensis, Enterobacter asburiae, Exiguobacterium acetylicum, Serratia marcescens, Planomicrobium okeanokoites, Rhodobacter capsulatus and Rhodobacter sphaeroides (Hassan and Bano 2015; Zahir et al. 2003).

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Different genera related to the wheat rhizospheric microbiomes are Arthrobacter, Alcaligenes, Acinetobacter, Azospirillum, Methylobacterium, Bacillus, Burkholderia, Erwinia, Flavobacterium, Enterobacter, Lysinibacillus, Paenibacillus, Rhizobium, Serratia and Pseudomonas (Khalid et al. 2004; Verma and Suman 2018).

8.4

Wheat Microbiome Detection and Diagnosis

Both culturable and un-culturable techniques have been employed to wheat-­ associated microbes to study diversity of their association with wheat crops and also to know their distribution (Fig.  8.5). Particularly, surface sterilization and serial dilution techniques are used to isolate wheat endophytic and rhizospheric microbes (Forchetti et al. 2007; Suman et al. 2016a, b). The epiphytic microbes are isolated with the imprinting method and, alternatively, serial dilution, and then pour or spread plate methods are used in sequence to isolate the same (Akbari et al. 2007; Yadav et  al. 2015a, b; Suman et  al. 2016a, b). For isolation and enumeration of wheat microbiomes (eubacteria, archaea, fungi), the following specific methods are employed along with specific medium. The specific medium for isolation of heterotrophic microbes is nutrient agar; for Pseudomonads isolation, King’s B agar medium is used. Arthrobacter is isolated by growing it in trypticase soy agar media; soil extract agar is used for the isolation of

Microbiome assessment method

Plant, soil, fruit, leaf, flower, seed, etc.

Sampling from the plant

Community RNA, Protein, metabolite extraction

Community DNA extraction

Amplicon sequencing

Metagenome sequencing

Community structure and abundance

Metatranscriptome Metaproteome sequencing analysis

Community function

Fig. 8.5  The flowchart of the assessment of microbiomes

Metabolome analysis

Community activity

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soil-specific microbes. Bacillus and Bacillus-derived genera can be isolated by T3A with heat treatment methods. Any chemically defined and complex medium is used for the isolation of archaea. Rose Bengal media and potato dextrose agar is used for isolation of fungi (Forchetti et al. 2007; Verma and Suman 2018). Microbiome samples can be assessed either through community DNA extraction or community RNA extraction. Community DNA extraction is sequenced through PCR amplification (16S–18S rRNA, ITS, cpn60) or amplicon sequencing and metagenome sequencing through which species, number, abundance and its composition are analysed; and the function of the community is assessed, respectively. Community RNA, protein and metabolite extraction can be done through meta-­ transcriptome sequencing, meta-proteome analysis and metabolome analysis from which the activity of the community is known (Liu et al. 2014).

8.5

Role of Wheat Microbiomes

The wheat microbiomes stimulate plant growth, soil health and fertility (Canbolat et al. 2006; Singh et al. 2007; Khan et al. 2007). Further, diverse abiotic stresses are ameliorated directly through the following: N2 fixation, production of siderophore and phytohormones (auxin, cytokinin and gibberellins) and solubilization of potassium, phosphorus and zinc (Sachdev et al. 2009; Kumar et al. 2001; Zaidi and Khan. 2005; Kudoyarova et al. 2014; Rroco et al. 2003). The same stresses are ameliorated indirectly through the following: production of ammonia, hydrogen cyanide, iron-­ chelating compounds, hydrolytic enzymes, antibiotics and antagonistic molecules for suppression of soilborne pathogens (Jankiewicz 2006; Scavino and Pedraza 2013; Upadhyay et al. 2012). Plant growth-promoting microbes produce phytohormones or plant growth regulators (Glick 2015) for better growth of the plants. Phytohormones are metabolites derived from bacteria such as Azotobacter, Bacillus, Azospirillum and Pseudomonas which show benefits such as promotion and spread of root development; with these benefits, roots of the plants increase their ability to uptake water and nutrients from soil in an efficient manner (Mehnaz 2015). Nitrogen-fixing microbe Azospirillum brasilense produces small amount of phytohormones like gibberellins, indole-3-acetic acid (IAA) and substances like cytokinin. PGP microbial strains like Azospirillum, Pseudomonas and Bacillus produce phytohormone like auxin which modulates shoot elongation and similar plant physiological processes and further promotes root development in plants (Verma et al. 2016). IAA and related compounds are also present, and these are demonstrated in many diazotrophs such as Acetobacter diazotrophicus, Azospirillum, Azotobacter, Paenibacillus and Polymyxa sp. (Timmusk et al. 2014; Aarab et al. 2015). Plants produce soluble organic compounds such as chelators and phytosiderophores which help to bind iron (Fe3+) and are made available in solution (Sarode et  al. 2009; Rroco et  al. 2003). Further, chelators’ produced ferrous ion (Fe3+) is reduced to ferric ion (Fe2+) and absorbed immediately on the root surface. Phytosiderophores are low molecular weight and are ferric ion-specific ligands.

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Thus, by production and discharge of phytosiderophore, PGPR are able to prevent the proliferation of phytopathogens which in turn facilitates plant growth (Mehnaz 2015; Sarode et al. 2013; Solanki et al. 2014; Jog et al. 2014).

8.6

Plant Growth-Promoting Bacteria (PGPB)

Plant growth-promoting substances such as rhizospheric or endophytic bacteria show beneficial effects in plant growth (Santoyo et  al. 2016; Kushwaha et al. 2020b). Plant growth-promoting substances extend over plant roots and the soil in vicinity and show direct or indirect effect on plants (Glick 2012; Santoyo et al. 2012, Gupta et al. 2015). The elements such as nitrogen, phosphorus and iron are available by plant growth-promoting bacteria, which are very much needed for plant growth and development (Calvo et al. 2014) (Fig. 8.6). Further, PGPB modulates level of hormones in the production of phytohormones like auxins, cytokinins and gibberellins (Yadav et  al. 2017a, b). PGPB are also able to reduce the levels of the ethylene phytohormone by synthesizing an enzyme, 1-aminocyclopropane-1-carboxylate (ACC) deaminase, that slices the ACC compound. ACC is a precursor compound of ethylene in higher plants (Glick et al. 1998; Yadav et al. 2016).

Phyllosphere Isolation of bacteria and characterization

Endosphere

Culture dependent method

Rhizosphere Molecular characterization

Plant growth associated functions

Direct

Indirect

Nitrogen fixation Mineral solubilization (P, K, Zn) Phytoharmone production (IAA, GA, SA, Cytokinin)

ACC deaminase Siderophore

Plant defense activation by antioxidants Hydrolytic enzyme production Antifungal volatile HCN Ammonia secretion

Extraction of DNA PCR amplification of genes (16S rRNA, rpoA, rpoB, gyrA, gyrB, etc.)

Sequencing and NCBI blast

Percent homology based identification and phylogenetic analysis

Fig. 8.6  A schematic representation of the isolation and characterization of plant growth-­ promoting bacteria

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Fig. 8.7 Plant-microbe interactions and their action of plant growth promotion

PGPB

Environmental factors

Secondary metabolites Space

Pathogen

Nutrient

Enhancement soil nutrient

Plant

After plant pathogen infection, PGPB decreases plant damage by indirect mechanism and thus promotes plant growth (Fig. 8.7). This is being demonstrated because of the inhibition of the pathogens which is induced by PGPB (Santoyo et al. 2012, 2016). Generally, the mechanisms are synthesis and release of antibiotics (such as 2,4-diacetylphloroglucinol); bacteriocins; chitinases; lipopeptides like iturin A, bacillomycin D and mycosubtilin; proteases; siderophores; and volatile organic compounds (Santoyo et al. 2012; Glick 2012) (Table 8.1). As already stated earlier, wheat microbiomes (phyllospheric, endophytic and rhizospheric) such as Azotobacter, Achromobacter, Alcaligenes, Azospirillum, Enterobacter, Herbaspirillum, Methanospirillum, Klebsiella, Pantoea, Burkholderia, Bacillus, Paenibacillus, Lysinibacillus, Methylobacterium, Pseudomonas, Rhodosporidium, Serratia, Staphylococcus, Penicillium, Streptomyces and Thermomonospora are isolated and characterized for plant growth promotion (Cakmakci et al. 2017).

8.7

Phosphate Solubilization and Mineralization

Phosphorus is an important plant major nutrient which follows nitrogen. Microorganisms undergo a sequence of processes that transform soil phosphorus (P), and thus they are considered as integral part of soil phosphorous cycle. But, application of huge amount of soluble inorganic phosphate into soil is fixing it as insoluble phosphate, and hence they become unavailable to the plants (Yadav et al. 2015a, b; Sharma et al. 2011a, b). Soil microbes have the capacity to change insoluble forms to soluble forms which are desired by plants for absorption. This is done by producing organic acids such as acetic acid, lactic acid, glycolic acid, formic acid, propionic acid, succinic acid and fumaric acid. Plants absorb only inorganic P so that bacteria take action to hydrolyse the organic P compounds with the help of the phosphatase enzyme that originates from their roots (Yadav et  al. 2015a, b). This enzyme also helps in

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Table 8.1  Microbes from different wheat niche involved in plant growth regulation Wheat microbe Bacillus, Azospirillum, Azotobacter Azospirillum brasilense Klebsiella pneumoniae Pseudomonas, Azospirillum, Bacillus Paenibacillus, Polymyxa, Acetobacter Pseudomonas sps.

Providencia sp. PW5

Acinetobacter calcoaceticus Pseudomonas putida

Azotobacter chroococcum Pantoea agglomerans Azorhizobium caulinodans Bacillus sp. (AW1) Providencia sp. (AW5) Brevundimonas diminuta (AW7) Bacillus thuringiensis Azotobacter chroococcum Paenibacillus ehimensis Pseudomonas pseudoalcaligenes Pseudomonas spp. Bacillus sp.

Pseudomonas denitrificans Pseudomonas rathonis Azotobacter chroococcum Pantoea agglomerans

Source and its application towards plant Rhizosphere Nutrient and water uptake from soil Nitrogen-fixing microbe Gibberellin and IAA production PGPB Cytokinin production Diazotrophs IAA and related compounds Rhizosphere Phosphorous solubilization, siderophore, IAA, DAPG Rhizosphere HCN, IAA, P solubilization, Zn solubilization Rhizosphere P solubilization, siderophore, IAA Produces several types of antibiotics, siderophores and slight quantity of hydrogen cyanide (HCN) Gibberellic acid (GA) IAA

References Verma and Suman (2018) El-Razek and El-Sheshtawy (2013) Verma and Suman (2018) Timmusk et al. (2014) and Aarab et al. (2015) Roesti et al. (2006)

Rana et al. (2012)

Prashant et al. (2009) Flaishman et al. (1996)

Narula et al. (2006)

N fixation

Sabry et al. (1997)

P solubilization, N2 fixation, ACC deaminase, siderophore, ammonia, HCN

Rana et al. (2011)

Higher heavy metal resistance Siderophore, indole acetic acid, HCN, P solubilization

Kumar et al. (2015)

IAA, P solubilization, rhamnolipids, siderophores Indole-3-acetic acid Antioxidant defence system SOD shoots and roots Shoot POD and CAT Gibberellic acid (GA), IAA, and auxin

Mishra et al. (2009) Wang et al. (2013)

Narula et al. (2006) and Egamberdiyeva and Höflich (2003)

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mineralization of organic phosphorous compounds. Through production of organic acids, chelation and exchange reactions process, the phosphorous-solubilizing bacteria convert insoluble inorganic P to a form available to plants (Yadav et al. 2015a, b). Mostly in soils, one can find a range of percentage of required amount of phytates which are organic P forms roughly 10–50% of phosphorous, and phytases should be mineralized to make ready supply of P to the plants (Singh et al. 2014). Reports showed that P solubilization is positive during their study on Alcaligenes sp., Providencia sp., Bacillus sp. and Brevundimonas (Verma and Suman  2018). Role of PGP microbes is very much observed in producing phosphatase, β-gluconase, dehydrogenase and antibiotics. Phosphate and other nutrient solubilization improved soil structure with stabilized soil aggregates (Verma and Suman 2018).

8.8

Biological Nitrogen Fixation

Through biological nitrogen fixation, 60% of available nitrogen on this earth is fixed (Verma et al. 2010). This fixation is alternative to chemical fertilizers and hence an economically beneficial and environmentally friendly alternative (Islam et al. 2002, Venieraki et al. 2011). The above-said process of nitrogen fixation is done by nif genes, i.e. coded form of the nitrogenase enzyme. In the case of nitrogen-poor soils, Azospirillum sp. is isolated, and it is diazotroph for nitrogen fixation (Hegazi et al. 1998; Verma and Suman 2018). Members of these bacterial genera have the ability in fixing atmospheric nitrogen. Symbiotic N2-fixing Rhizobium and others like Azospirillum are some microbial groups which fix nitrogen by colonization of root zones. Actinomycetes in non-leguminous trees and free living N2 fixers as blue green algae, Bacillus, Acetobacter, Klebsiella, Azotobacter and Pseudomonas are also helping nitrogen fixation (Prasanna et al. 2012).

8.9

Biological Control

To prevent the proliferation of plant pathogens, a variety of antibiotics are identified and are having compounds such as amphisin, 2,4-diacetylphloroglucinol (DAPG), phenazine, oomycin A, pyoluteorin, tensin, pyrrolnitrin, tropolone, cyclic lipopeptides produced by Pseudomonads and oligomycin A, kanosamine, zwittermicin A and xanthobaccin produced by Bacillus, Streptomyces and Stenotrophomonas sp. (Verma and Suman 2018). Many bacterial genera such as Agrobacterium (Hammami et  al. 2009), Arthrobacter (Banerjee et  al. 2010), Azotobacter (Kannan and Sureender 2009), Bradyrhizobium (Akhtar et  al. 2010; Mishra et  al. 2009), Bacillus, Enterobacter (Wang et al. 2012; Solanki et al. 2012; Kushwaha et al. 2019; Singh et al. 2014), Burkholderia (Santiago et al. 2014) and Pseudomonas (Solanki et al. 2015; Goswami et al. 2013) have shown their potential in biocontrol under in vitro and in vivo conditions, and they are able to resist soilborne fungal pathogens (Table 8.2).

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Table 8.2  Microbes involved in biological control Microbiome genera Bacillus, Enterobacter sps.

Antagonist against Rusts of wheat

Verticillium lecanii, Erwinia herbicola, Pseudomonas aurantiaca Verticillium lecanii + Paecilomyces fumosoroseus, Beauveria bassiana Pseudomonas putida

Flaishman et al. (1996) and Peng et al. (2014) Eldoksch et al. (2001), Kalappanavar et al. (2008) and El-Sharkawy et al. (2015) Ghoneem et al. (2015)

Trichoderma harzianum, Streptomyces viridosporus, Bacillus subtilis, Saccharomyces cerevisiae Combined application of arbuscular mycorrhizal fungi and Azospirillum amazonense T. harzianum

B. subtilis NJ-18 Combined application of yeasts like Rhodosporidium kratochvilovae strain UM350, Cryptococcus laurentii strain UM108 and Aureobasidium pullulans strain LS30 Bacillus subtilis strain E1R-j

Bacillus subtilis BTS 3, B. amyloliquefaciens BTS 4, Staphylococcus saprophyticus BTS 5 and B. amyloliquefaciens BTLK6A B. subtilis D1/2 (DAOM 231163) and B. subtilis RC 218, Brevibacillus sp. RC 263, Bacillus amyloliquefaciens Lysobacter enzymogenes strain C3 Cryptococcus, Brevibacillus sp. RC 263 Clonostachys rosea strain ACM941 (CLO-1) FHB

References Wang et al. (2012) and Li et al. (2013) Alien (1982), Srivastava (1985), Kempf and Wolf (1989), and Wang (2011) Hall (1981)

Tan spot, spot blotch and Helminthosporium leaf blight, Fusarium head blight of wheat and septoria blotch Sharp eye spot Powdery mildew of wheat

Fusarium head blight disease of wheat and powdery mildew of wheat Wheat blast and black point complex of wheat

Fusarium head blight of wheat; take all disease of wheat

Fusarium head blight of wheat

Perelló et al. (1997), Monte (2001), Hossain et al. (2015), and Mahmoud (2016) Peng et al. (2014) Curtis et al. (2012)

Gao et al. (2015) and Mahmoud (2016) Surovy et al. (2017) and El-Gremi et al. (2017)

Chan et al. (2003), Nasraoui et al. (2007), Crane et al. (2014), Palazzini et al. (2016) and Liu et al. (2009) Jochum et al. (2006) Schisler et al. (2002, 2006, 2014) Xue et al. (2014) (continued)

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Table 8.2 (continued) Microbiome genera Pseudomonas fluorescens (strains MKB 158 and MKB 249) and P. frederiksbergensis (strain 202) Aureobasidium pullulans

Antagonist against Karnal bunt of wheat

Wachowska and Głowacka (2014) Sharma and Basandrai (2000)

Trichoderma viride, T. harzianum and Gliocladium deliquescens Trichoderma pseudokoningii, T. lignorum, T. koningii, G. deliquescens and G. virens, Azotobacter chroococcum Trichoderma viride, Gliocladium deliquescence, T. harzianum, Pseudomonas fluorescence and Bacillus subtilis Bacillus megaterium B5, B. amyloliquefaciens B28, T. harzianum T37 and Epicoccum sp. E52 Streptomyces, Bacillus, Pseudomonas fluorescens, P. putida, Pseudomonas chlororaphis MA 342, Gliocladium and Trichoderma harzianum Phialophora radicicola var. radicicola

Amer et al. (2000)

Loose smut of wheat and black point complex of wheat

Black point complex of wheat

Agarwal and Nagarajan (1992), Singh and Maheshwari (2001), Monaco et al. (2004) and El-Meleigi et al. (2007) El-Meleigi et al. (2007)

Common bunt disease of wheat

Borgen and Davanlou (2000), McManus et al. (1993) and Kollmorgen and Jones 1975

Take all disease of wheat

Wong and Southwell (1980), Wong et al. (1996) and Mathre et al. (1998) Simon and Sivasithamparam (1989) and Zafari et al. (2008) Barnett et al. (2017)

Trichoderma koningii, T. harzianum, T. viride Pandoraea apista (S18 and S19) and Cylindrocarpon destructans S22

References Khan and Doohan (2009) and Vajpayee et al. (2015)

Rhizoctonia root rot disease of wheat

Bacillus amyloliquefaciens is understood for lipopeptide and polyketide production for biological management and plant growth promotion activity against soilborne pathogens. Some bacteria also are capable of producing volatile compound referred to as hydrogen cyanide (HCN) for biocontrol of black root rot of tobacco, caused by Thielaviopsis basicola; also reported is the production of DAPG and HCN by Pseudomonas contributing to the biological management of bacterial canker of tomato (Sacherer et al. 1994; Lanteigne et al. 2012). Wheat microbiome bacteria can reduce virulence of a plant pathogenic fungus by altering histone acetylation (Chen et  al. 2018). The molecular mechanisms between Pseudomonas piscium bacterium isolated from the wheat head microbiome and the plant pathogenic fungus Fusarium graminearum have revealed that a compound secreted by the bacteria (phenazine-1-carboxamide) directly affects the activity of fungal protein FgGcn5, which is a histone acetyltransferase of the

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Spt-­Ada-­Gcn5-acetyltransferase (SAGA) complex which led to deregulation of histone acetylation in F. graminearum and subsequently suppression of fungal growth and virulence and biosynthesis of mycotoxin. Thus, it has been proven that an antagonistic bacterium can inhibit growth and virulence of a plant pathogenic fungus by manipulating fungal histone regulation (Chen et al. 2018). According to Liu et al. (2017), effects of jasmonic acid signalling on the wheat microbiome differ between body sites. The influence of jasmonic acid (JA) on the diversity and function of wheat microbiome and whether there is any specificity of the influence with respect to plant part were determined. By exogenous application of methyl jasmonate, JA pathway was activated and was confirmed by significant increases in the abundance of JA signalling-related gene transcripts. Phylogenetic marker gene sequencing revealed that JA signalling reduced the diversity and changed the composition of root endophytic, but the composition of shoot endophytic or rhizospheric bacterial communities was unchanged. But the total enzymatic activity and substrate utilization profiles of rhizosphere bacterial communities were not affected by JA signalling. Therefore, the conclusion drawn after this study was that JA signalling on the wheat microbiome is specific to individual plant parts.

8.10 W  heat Microbiome Under Different Stress Conditions and Advance Research Till date, the status of wheat microbiome research is at budding stage. However the research in the following aspects has provided insights, and the work presented here provided a way forward to study fundamental microbiome research with the aim of better understanding of identification of potentially beneficial microbes, their dynamics and their role in reducing the pathogen pressure and improving plant yield. To successfully reach the goals in the microbial research, the composition of plant-associated community that can fulfil the required need in plant disease management and in sustainable management has to be determined.

8.10.1 Performance of Microbiome Under Nutrient Stress Status Very recently Page et  al. (2019) described the microbiome profiling of Triticum aestivum under nitrogen- and phosphorus-starved situations. As wheat farming consumes approximately 20% of the worldwide production of inorganic N and P fertilizers and keeping in view the fact that plants have natural partnerships with microbes that can enhance their nitrogen (N) and/or phosphorus (P) acquisition, it is essntial to evaluate the association between wheat and its microbes in boosting N/P availability. They have tested whether N/P-starved Triticum aestivum showed microbiome profiles that are similarly different from those of N/P-amended plants in their own bulk soils. The conclusions drawn that six N/P starvation and plant specific microbial communities that may represent the attraction of microbes towards T. aestivum when it experiences N/P starvation. However, additional research will be needed to validate this interpretation under different climatic conditions. But the

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work done helps to keep a step forward. Identification of the potential T. aestivum partners give us a target list for subsequent relationship-assessing  microbioata for boosting yields of the crop and therefore need to be standardized in farmers field with common package of practices. Microbiome enhances N and P uptake  and experimently proved by Panwar and Singh (2000). A. chroococcum and P. agglomerans like microbe not only enhance P and K uptake but also increase plant growth and plant dry matter (Narula et al. 2007, Islam et al. 2002). Application of biofertilizers also reported to enhance the accumulation of nutrient in wheat crop by different scientists (Khan and Zaidi 2007; Abbasi and Yousra 2012). Not only macronutrient, but microbiomes also provide positive impact on the availability of essential micronutrients of wheat (Jog et al. 2014; Mishra et al. 2011; Yasin et al. 2015).

8.10.2 Performance of Microbiome Under Drought Condition In the introduction, it is already mentioned that areas in South Asian countries are suffering from drought. Here microbiomes could be a good supplement to overcome this stress as they counteract with damage due to water stress. Rhizosphere biology mainly influences on the productivity of plants (Watt et  al. 2006; Richardson et al. 2009 and Berendsen et al. 2012). Plant growth-promoting (PGP) strains of Azospirillum and Herbaspirillum have been reported to colonize Brachypodium roots and enhance growth of some Brachypodium genotypes under low or no nitrogen conditions (Amaral et al. 2016). Another group of scientists also used the PGP strain Bacillus subtilis B26 to increase Brachypodium biomass and improve plant drought resistance (Gagne et al. 2015). Also some microbiome provided a better water status in osmotic stress condition on wheat plant (Chakraborty et al. 2013; Pereyra et al. 2012). Artificial inoculation of Azospirillum brasilense sp. 245-primed wheat seed can sustain under water stress condition by increasing the apoplastic water function in both shoot and root compared to noninoculated wheat plant (Creus et al. 2004).

8.10.3 Performance of Microbiome Under Stress Cultivation System Nowadays governments are gearing towards conservation agriculture. So another selection criteria for microbiome that they can survive under stress cultural practices or minimal management approaches. A long-term field experiment demonstrates the influence of tillage on the bacterial potential to produce soil structure-stabilizing agents such as exopolysaccharides and lipopolysaccharides (Cania et al. 2019). The non-metric multidimensional scaling (NMDS) ordination plot showed a difference between the composition of bacterial families from the deepest sampled soil layer and the uppermost soil layers. It was revealed that there is no clear separation of the tillage treatments like the effects of tillage, depth and

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their interaction on the general microbial community structure. Even salicylic acid signalling in wheat microbiome also depends on soil type and on strategic tillage (Liu et al. 2016). Another study by Hartman et al. (2018) revealed that cropping practices manipulate abundance patterns of root and soil microbiome members. The soil and wheat root microbiomes under conventional and organic managements with different tillage intensities were conducted to analyse the effects of management type and tillage on microbial communities  as well as their infulence on various  ecosystem processes and regulations. The study revelaed that the microbial communities play an important roles in nutrient cycling via decomposition of organic matter, and transformation and fixation of soil nutrients like nitrogen and phosphorus. It was revealed that there was pronounced influence of cropping patterns on microbial community composition which were specific for the respective microbiomes. In roots, management type was the important factor for bacteria when compared with fungi, and this is generally determined by changes in tillage intensity. There were many taxonomically diverse cropping-sensitive microbes, in which their response practices are specific. Cropping practices may allow manipulation of influential community members in which members co-occurring with many other microbes in the community. Understanding the patterns of cropping-sensitive microbe abundance helps in developing microbiota management strategies for smart farming. Even the soil microbiomes perform better in non-suppressive soil than suppressive soil (Hayden et al. 2018). The comparative metatranscriptomic approach was applied to assess the taxonomic and functional characteristics of the rhizosphere microbiome of wheat plants grown in adjacent fields which are suppressive and non-suppressive to the plant pathogen R. solani AG8. Soils collected prior to sowing showed similar inoculum levels of the pathogen R. solani AG8 in both the suppressive and non-suppressive fields, as determined by quantitative PCR. The inoculum was observed in both fields throughout the cropping season, in particular during the initial 8  weeks of crop growth. The inoculum potential was more in the non-­ suppressive soils compared to that in the suppressive soils, resulting in significantly higher R. solani AG8 DNA in the non-suppressive soils, and the disease index was higher in non-suppressive soil compared to suppressive soils. The status of wheat microbiome under different management strategies and potentiality of endophytes in disease protection were studied by Gdanetz and Trail (2017) in detail. They analysed the fungal and bacterial communities of leaves, stems and roots of wheat throughout the growing season across growth stage and four crop management strategies like organic, low input, no till and conventional using 16S and fungal internal transcribed spacer region gene amplicon sequencing, and endophytes were isolated from plants and are tested for antagonistic activity against wheat pathogen Fusarium graminearum, and also antagonistic strains were assessed for plant protective activity in seedling assays. But contrary to the expectations based on the previous studies on different management strategies, management strategy does not show a strong influence on the plant microbial communities.

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A meta-analysis was done to determine whether plant domestication affects the composition of the root-associated microbiome (Jaramillo et al. 2018). The significant and consistent differences in the abundance of Bacteroidetes, Actinobacteria and Proteobacteria for different plant species were observed. The higher relative abundance of different bacterial families on the roots of wild relatives of the different plant species was observed. For conducting this study, it is emphasized that the same computational pipeline was used by adopting a rarefaction of the operational taxonomic unit (OTU) table to the same sequencing depth and also found similar differences between the prokaryotic composition of the rhizosphere microbiome of wild and domesticated plant species with a significantly higher abundance of Bacteroidetes in the roots of wild plant relatives. However, the reasons behind the relative abundance of Bacteroidetes in the root and rhizosphere compartments of wild relatives of various crop plant species are yet unknown. Therefore, their prevalence in the root compartments of wild plant species may be a phylogenetic signal associated with the presence of complex biopolymers in the root exudates (Table 8.3).

8.10.4 Role of Microbiome to Trigger Flowering Sometimes microbiomes have strong influence on the crop physiology like timing of flowering (Lu et al. 2018). The rhizosphere microbial communities can modulate the timing of flowering of Arabidopsis thaliana. The abundance of rhizosphere microorganisms and prolonged nitrogen bioavailability by nitrification, delayed flowering by converting tryptophan to the indole acetic acid (IAA), thus downregulating genes that trigger flowering, and stimulating plant growth. Lu et al. (2018) also observed a novel metabolic network in which soil microbiota influenced plant flowering time, thus providing a water font on the key role of soil microbiota on plant functioning and thus helping to mitigate the effects of climate change and environmental stress on plants using microbiomes.

8.11 Future Prospectives and Conclusion Over the last 150 years, plant pathologists only dealt with individual microbes that have adapted to specific niches on their hosts. Now we need to think more to perform high-throughput sequencing of these niches to explore microbial communities that can affect disease outcomes. A fundamental understanding of the plant microbiome is necessary for their successful execution amongst the farmers. The rhizospheric microbiomes are regulated by root exudates, selection of plant genotype and adoption of environment. So, plant microbiome must be a part of future breeding programmes so that next-generation plant genotypes have enhanced ability to interact with beneficial microbes either of natural soil microbiota or of microbial inoculants. Worldwide many wheat cultivars that are biofortified, for

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Table 8.3  Microbes involved in amelioration of various stresses Wheat microbes Azospirillum lipoferum Bacillus thuringiensis Bacillus safensis, Ochrobactrum pseudogregnonense Bacillus sp. Bacillus aerophilus, Lysinibacillus sphaericus Azospirillum brasilense INTA Az-39 wheat roots

Bacillus amyloliquefaciens and Azospirillum brasilense Pseudomonas fluorescens, Pantoea agglomerans, Mycobacterium sp. Pseudomonas fluorescens 153, 169, Pseudomonas putida 108 Achromobacter xylosoxidans, Serratia marcescens Pseudomonas putida N21, Pseudomonas aeruginosa N39 and Serratia proteamaculans M35 Azospirillum sp. Pseudomonas putida, Pseudomonas extremorientalis, Pseudomonas chlororaphis and Pseudomonas aurantiaca Bacillus thuringiensis, Azotobacter chroococcum, Paenibacillus ehimensis, Pseudomonas pseudoalcaligenes Bacillus megaterium M3, Bacillus subtilis OSU142, Azospirillum brasilense Sp245, Raoultella terrigena

Stress Drought Heavy metal Drought Cold stress Acid and alkalinity stress Drought

Temperature

References Naveed et al. (2014) Kumar et al. (2015) Chakraborty et al. (2013) Sezen et al. (2016) Verma et al. (2016) Diaz-Zorita and Fernández-Canigia (2009) Abd-Alla et al. (2013) Egamberdiyeva and Höflich (2003)

Salinity Barra et al. (2014) Zahir et al. (2009) Nabti et al. (2010) Abbaspoor et al. (2009) Heavy metal

Kumar et al. (2015)

Cold

Turan et al. (2012)

example, rich in iron, rich in zinc, rich in anthocyanin, etc., are already released and also popular. In this scenario not only the microbial but also the host part of the interactions need to take more attentions, since the associated microbiome is emerging as a fundamental trait for controlling plant biotic and abiotic stress and optimizing plant growth promotion (Bulgarelli et al. 2013; Sclaeppi and Bulgerelli 2015). In the case of managing pathogen burden, the combined deployment of beneficial services of the plant microbiome (agricultural probiotics) and innate immune functions (resistance genes) is expected to deliver durable and sustainable protection from disease (Dangl et al. 2013). Identification of the genetic components of the host-microbiome control will be key factor for its ultimate inclusion into breeding programs. Developing the next-generation agricultural tools and practices will be dependent on integration of all covariates present in agro-ecosystem. Under a specific agro-climatic condition, the performance of native soil microbiome and inoculated microbiome sometime interact with one or both with individual plant species and

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genotype, and this interaction drastickly  influence the  performance of the crop. Hence, we can exploit the use of plant microbiome at work and next-generation agriculture in reality to solve the aforesaid multivariate equations. The ultimate goals of the researchers for the fate of the farmers are to minimize the use of fertilizers, protect plants from chemicals as well as reduce the cost of cultivation in the era of sustainable agriculture. But to reach this goal, we need to know the fundamental relationships between microbes and microbes and wheat plants and microbes and how much longer this relation may work under changing climatic conditions. Knowledge gain from this chapter will help to understand the selection criteria of microbes for alternative use of microbiomes as fertilizers, biocontrol agent, growth promoters and in efficenet  soil nutrient cycling. But need more depth of researches for long duration under different cropping systems  to translate microbiome concept in agriculture. Cropping practice and microbiome engineering would help only in sustainable agriculture system. Due to intensive cultivation, soil just become empty of nutrients  and the  physical and biological health of the existing soil hamphered badly. The microbiome is a fundamental part of basic processes such as plant development or growth of essential organs such as the root and for improved acquisition of nutrients and water; the mentioned capabilities make the microbiome an important component for the plant to carry out physiological functions. Analysis of metagenome and comparison with plant-­ associated communities will lead to novel phylogenetic and functional insight. The application of microbial inoculants to the field presents one of the several conceivable next-generation agricultural tools or practices.

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9

Entomopathogenic Fungi: A Potential Source for Biological Control of Insect Pests Anjney Sharma, Ankit Srivastava, Awadhesh K. Shukla, Kirti Srivastava, Alok Kumar Srivastava, and Anil Kumar Saxena

Abstract

Insect pests with high population level are inimical and cause enormous damage to agricultural crops and economy as well as decrease the food security for the growing human population. For controlling insect pests, the use of entomopathogenic fungi (EPF) is very much useful, and it was developed as eco-friendly mycopesticide that is useful in the regulation of insect pests. These entomopathogenic fungi have a unique mode of infection on different orders of insects. Recently, it was investigated that in addition to insect pest control, these entomopathogenic fungi also act as endophytes and biocontrol agents of plant pathogens and promote plant growth as rhizosphere fungi. Numerous environmental abiotic and biotic factors are recognized to inhibit or enhance the fungal efficacy against the insect pathogens. Advanced research in the genome biology of pathogenic insect fungi has shown that genetic features of these organisms are developed for fungal adaptation with various host insects. The efforts toward genetic engineering of entomopathogens, the knowledge of its virulence and tolerance to adverse conditions will potentiate cost-effective applications of mycoinsecticides for pest control in the agricultural fields. The studies suggest that the exploitation of ecological, genetic and functional diversity of these fungi increases our potential for integrated pest management. Consideration of the insect microbiome in fungal insect pathology represents a new frontier which may contribute in deciphering the obscure pathological aspects of the biology of entomopathogenic fungi and its ecology. Taking these into account, in the present chapter, we highlight the importance, classification, mode of action, factors affecting its virulence effiA. Sharma (*) · A. Srivastava · K. Srivastava · A. K. Srivastava · A. K. Saxena ICAR-National Bureau of Agriculturally Important Microorganisms, Mau Nath Bhanjan, Uttar Pradesh, India A. K. Shukla K. S. Saket P. G. College (Dr. Rammanohar Lohia Avadh University), Ayodhya, Uttar Pradesh, India © Springer Nature Singapore Pte Ltd. 2020 M. K. Solanki et al. (eds.), Phytobiomes: Current Insights and Future Vistas, https://doi.org/10.1007/978-981-15-3151-4_9

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cacy, the role of genetic engineering in strain improvement, and ground level of entomopathogenic fungi for integrated pest management (IPM), and plant growth promotion with commercial available entomopathogenic products is critically discussed. Keywords

Entomopathogenic fungi · Genetic engineering · Insect pests · Integrated pest management · Virulence

9.1

Introduction

Due to the dependency of the market at a global scale to agricultural merchandise, leading-edge technology in agriculture is increasingly used that is required to develop new agricultural practices and has potential to alleviate the adverse negative effects on the ecosystem and consequently results in the production of valuable safe products for human consumption. However, there is a major constraint in increasing agricultural production yield due to loss caused by insect pests, plant diseases, weeds, etc. (Oerke et al. 1994). In evolutionary agricultural practices, pest problems are unavoidable and arise largely due to simplified agroecosystems and additionally because of the creation of less stable natural ecosystems. It is investigated that insect pests such as locusts, grasshoppers, termites, and cattle ticks have caused huge economic and agricultural production losses, that is, about 40%, in many parts of the world (Thacker 2002; Chandler et  al. 2011). Although the use of pesticides has increased marginally, crop losses have remained relatively stable (Oerke 2006). Various industrialized nations are trying to shift their strategy to using transgenic plants that express particular traits like resistance to insects, fungi, or viruses for pest management. Several agrochemicals pesticides are still being used by farmers for the control of insect pests and diseases in their agricultural practices. They have been responsible for maintaining and increasing the quality and quantity of food and fiber worldwide. The extensive use has resulted to adverse effect on nontarget organisms, deposition on edible food crops, groundwater pollution, and resistance of insects against the chemicals, and negative effect on human health has forced scientists to focus on the development of alternative environmentally safe strategies that are cost-effective and reliable. Integrated pest management (IPM) is a comprehensive approach to crop production (Chandler et al. 2011). This is a shift from the traditional individual pest-centered strategies that relied heavily on chemical pesticides to a more holistic approach of viewing the entire crop production system as a whole and managing rather than eradicating the pests. In line with this point, several microbial agents have been developed to manage insect pests. Entomopathogenic fungal biological plant protection plays a key role in the program of sustainable pest management. For integrated pest management, ready-made use of entomopathogenic fungus as biocontrol agents to control the insect density and increase the crop yield has several benefits compared with conventional insecticides. These

9  Entomopathogenic Fungi: A Potential Source for Biological Control of Insect Pests

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encompass low expenses, high performance, safety for beneficial organisms, reduction of residues within the environment, and accelerated biodiversity (Asi et  al. 2013; Gul et  al. 2014). Entomopathogenic fungus has been known as important inhibitory factor of plant bugs for more than a century and is continuously used in pest biocontrol management throughout the world (Jaber and Enkerli 2017). Entomopathogenic fungi fill an extremely important niche and are well suited for development as microbial biopesticides for control of the harmful insect pests. Almost all orders of insects are susceptible to fungal sicknesses. Entomopathogenic fungi are potential eco-friendly biocontrol agents especially because of their excessive reproductive abilities, goal-specific activity, minimal impacts on beneficial and other nontarget organisms, brief era time, and resting stage or saprobic phase—generating competencies which can make sure their survival for an extended time when no host is present (Mudgal et al. 2013). Entomopathogenic fungi can be found in a wide range of environmental conditions (including arid to tropical settings, terrestrial to aquatic habitats, and arctic to temperate climates), possess potential to colonize a wide variety of plant species, and infect a broad array of insects (Meyling et al. 2012; Mantzoukas et al. 2015). Researchers have stated that approximately a thousand species of fungi are identified as causal agents of disease in arthropods (Goettel et al. 2010; Vega et al. 2012). The majority of entomopathogenic fungi used for biological control of insects and mites are in the orders Hypocreales and Entomophthorales. Most of the biological control fungi produced commercially are included in Hypocreales. Various other fungi such as Metarhizium spp., Beauveria bassiana, Lecanicillium spp., and Isaria fumosorosea are being used against a large number of pests in different variety of crops. About 170 fungal formulations from at least 12 species of fungi have been developed (Faria and Wraight 2007). It is believed that there are about more than 750 species of fungi that have been identified to cause various infections in insects. Most of the entomopathogenic strains or species are obligate pathogens that show specific ecomorphological adaptations of their host’s life cycles, such as the production of infective spores that are produced on insect cadavers during the night. These fungi often cause natural epizootics in insect and mite populations. Natural epizootics of entomophthoralean fungi are being used as a natural form of pest control. Pioneering work of Inglis et al. (2001) conducted with Beauveria bassiana (Balsamo) and Vuilleminia (Ascomycota: Hypocreales), as entomopathogenic endophytes and ubiquitous soilborne fungus and one of the most commercialized fungal biopesticides, reveals that they infect >700 insect species. A number of recent studies reveal that entomopathogenic fungi, often entirely taken into consideration as insect pathogens, play extra roles in nature, such as endophytism, plant disease antagonism, plant growth promotion, rhizosphere colonization, and management of various abiotic stresses (Vidal and Jaber 2015). Moreover, most studies investigating the interactions among plants and endophytic entomopathogens have up to now centered on the advantages of such interactions to the host plant through multiplied tolerance and resistance to biotic elements including pests and illnesses (Lopez and Sword 2015). Due to low virulence and inconsistencies of their performance within various field environmental stresses, currently, fungal pathogens have a small market share and small chances of

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killing insects in comparison to chemical insecticides (Fang et al. 2012). Low virulence may be incorporated as an evolutionary balance between microorganisms, and their hosts may have adapted to the pathogen to avoid rapid killing even at high doses, in which cost-effective biocontrol will require genetic modification of the fungi (Gressel 2007). Genetic engineering is an effective green device to improve the efficacy of mycoinsecticides by enhancing their virulence and tolerance to environmental stresses. Modern biotechnological tools that now enable genetic improvement of entomopathogens for myco-biocontrol of fungi are now feasible. Molecular biology techniques, coupled with the cloning of genes to express insect proteins and insecticidal proteins/peptides from insect pathogens, will create more effective strains for pest management. Further research is desirable under variable environmental conditions to monitor the environmental fate of recombinant fungal strains. Comparative genomics has facilitated the identification of fungal fitness characteristics and the selective forces acting on them to enhance our knowledge of why and how entomopathogenic fungi interact with insects and other additive components of their environment. So far, there may be plenty of extra-genomic facts on ascomycete insect pathogens, as sequences are available from Metarhizium strains, Beauveria bassiana, Cordyceps militaris, Ophiocordyceps sinensis (anamorph, Hirsutella sinensis), Ophiocordyceps unilateralis, Tolypocladium inflatum, and Hirsutella thompsonii (Zheng et  al. 2011; Xiao et  al. 2012; Bushley et  al. 2013; Pattemore et al. 2014; de Bekker et al. 2015; Agrawal et al. 2015). Molecular studies provided valuable information on the phylogenetic relationships with various other fungi. Hence, sequence data can, therefore, provide crucial information on how these organisms reproduce and persist in different environments (Wang and St. Leger 2014). It is important to understand the ecology of fungal entomopathogens. Further, it is reported that various entomopathogenic fungi play important roles in nature, such as endophytes, useful rhizosphere associates, antagonists of plant pathogens, and possibly even plant growth promoters. A growing quantity of research has currently established the ability of several entomopathogenic fungi after endophytic establishment to promote plant growth (Sasan and Bidochka 2012; Lopez and Sword 2015). Increased plant growth, mediated through colonization by fungal endophytes, is the outcome in the suppression of numerous abiotic and biotic stresses, consisting of plant diseases (Kuldau and Bacon 2008). Hence, it is an urgent need to review and understand how entomopathogenic fungi solely act as biopesticides and also promote plant growth. Keeping the above facts, we are trying to summarize the recent information regarding the role of entomopathogenic fungi in biocontrol and plant growth promotion. Additionally, the factors affecting the activities of entomopathogenic fungi are also being discussed.

9.2

Classification and Type of Entomopathogenic Fungus

In eukaryotes, the kingdom Fungi is a major group with approximately 700 described entomopathogenic fungi species (Roberts and Humber 1981) which represent